Bordetella avium Turkey Coryza (Rhinotracheitis) in Poultry

Etiology

Bordetella avium is a Gram-negative, aerobic, non-fermentative, motile coccobacillus belonging to the family Alcaligenaceae. The organism was originally classified as Alcaligenes faecalis but was reclassified based on cellular fatty acid analysis and DNA hybridization studies [1, 2]. B. avium is the primary etiologic agent of turkey coryza, also termed avian bordetellosis or infectious rhinotracheitis of turkeys. The bacterium produces several virulence factors, including a heat-labile toxin (HLT) and a heat-stable toxin (HST), both of which contribute to ciliostasis and epithelial damage in the upper respiratory tract [3, 4, 5]. The heat-labile toxin is a dermonecrotic toxin that induces local inflammation and necrosis, while the heat-stable toxin is associated with systemic effects [4, 5]. Plasmid profiling has shown no consistent correlation between plasmid carriage and pathogenicity [6]. B. avium-like bacteria have been isolated from other avian species but do not confer cross-protection in turkeys [7].

Bordetella avium Turkey Coryza Rhinotracheitis: Epidemiology

Turkey coryza is a highly contagious upper respiratory disease primarily affecting domestic turkeys (Meleagris gallopavo). The disease has been reported in major turkey-producing regions worldwide, including North America, Europe, the Middle East, and Asia. Epidemiological surveys have documented prevalence rates varying by region and management system. In Poland, serological and bacteriological monitoring revealed widespread circulation of B. avium in commercial turkey flocks [8]. In Iran, isolation and molecular identification confirmed the presence of B. avium in both commercial and backyard broiler turkeys [9]. A study in Egypt reported a prevalence of 18.5% in turkeys with respiratory signs, with high rates of antimicrobial resistance to commonly used drugs [10]. The bacterium is transmitted horizontally via aerosolized respiratory secretions, contaminated fomites, and direct bird-to-bird contact. Vertical transmission has not been demonstrated. Morbidity can approach 100% in naive flocks, while mortality is typically low (1-10%) unless complicated by secondary pathogens such as Ornithobacterium rhinotracheale or Escherichia coli [11]. Concurrent infections with Spironucleus meleagridis (hexamitiasis) or Cochlosoma anatis may exacerbate clinical signs.

Clinical Signs

The incubation period ranges from 5 to 10 days. Clinical signs are most pronounced in young poults (2-8 weeks of age) but can occur in older birds. The hallmark presentation is an acute onset of serous to mucoid nasal discharge, sneezing, rales, and conjunctivitis. Affected birds exhibit shaking of the head, frothy ocular discharge, and dyspnea. In severe cases, the infraorbital sinuses become distended with exudate, leading to facial swelling. Tracheal rales are audible on auscultation. Systemic signs include depression, anorexia, and reduced weight gain. Electrocardiographic abnormalities, including bradycardia and altered T-wave morphology, have been documented in experimentally infected poults, suggesting a direct or indirect effect of bacterial toxins on cardiac function [12]. Morbidity is high, but mortality is usually low unless secondary bacterial infections supervene. In breeder flocks, the disease may cause a transient drop in egg production and increased culling due to respiratory distress [11].

Pathology

Gross lesions are confined to the upper respiratory tract. The nasal passages, infraorbital sinuses, and trachea contain copious amounts of catarrhal to mucopurulent exudate. The tracheal mucosa is hyperemic and edematous, and in chronic cases, caseous plugs may obstruct the lumen. Microscopically, the hallmark lesion is deciliation and necrosis of the tracheal epithelium, accompanied by infiltration of heterophils and mononuclear cells. The lamina propria is edematous with congestion. Toxin-mediated ciliostasis is a key pathogenic mechanism; the heat-labile toxin causes detachment of ciliated epithelial cells, impairing mucociliary clearance and predisposing the host to secondary infections [3, 4]. In some cases, mild airsacculitis and pneumonia may be present if secondary pathogens are involved.

Diagnostics

A definitive diagnosis of Bordetella avium turkey coryza rhinotracheitis requires isolation or molecular detection of the bacterium from clinical specimens. Swabs of the nasal cavity, choanal cleft, or trachea are the preferred samples. Bacteriological culture on MacConkey agar or Bordet-Gengou agar yields small, lactose-negative, convex colonies after 24-48 hours of aerobic incubation at 37 degrees Celsius. Biochemical identification is based on oxidase positivity, urease negativity, and failure to ferment carbohydrates. However, phenotypic identification can be ambiguous, and molecular methods are now considered the gold standard.

Molecular Diagnostics

Several real-time PCR (TaqMan) assays have been developed and validated for the detection of B. avium. Hashish et al. [13] described two novel real-time PCR assays targeting the fla (flagellin) gene and the bcr (Bordetella avium-specific) gene, demonstrating high analytical sensitivity and specificity compared to the existing real-time PCR assay. The fla assay targets a conserved region of the flagellin gene, while the bcr assay targets a unique genomic region. Both assays showed 100% diagnostic sensitivity and specificity on a panel of clinical samples from turkeys. Register and Yersin [14] analytically verified a PCR assay targeting the 16S rRNA gene, which reliably differentiated B. avium from other Bordetella species and closely related organisms. Conventional PCR followed by sequencing of the 16S rRNA gene or the fla gene is also used for confirmatory identification [9, 10].

Serology

Serological testing using enzyme-linked immunosorbent assays (ELISAs) or microagglutination tests can detect antibodies to B. avium, but these methods are more useful for flock-level surveillance than for individual diagnosis. The heat-labile toxin neutralization test has been described for detection of neutralizing antibodies [3]. However, serology is limited by the lack of standardized commercial kits and the potential for cross-reactivity with other Gram-negative bacteria.

Differential Diagnosis

Turkey coryza must be differentiated from other respiratory diseases of turkeys, including:

Diagnostic Workflow

The following decision tree summarizes the recommended diagnostic approach for suspected B. avium infection:

flowchart TD
    A[Clinical signs: nasal discharge, sneezing, conjunctivitis in turkeys], > B[Collect choanal or tracheal swabs]
    B, > C{Initial screening}
    C, > D[Real-time PCR (fla or bcr gene)]
    D, > E{Result}
    E, >|Positive| F[Confirm with culture or alternative PCR target]
    E, >|Negative| G[Consider other pathogens: ORT, Mycoplasma, Avian influenza]
    F, > H[Report: Bordetella avium confirmed]
    G, > I[Perform differential diagnostic panel]
    I, > J[PCR for ORT, Mycoplasma gallisepticum, Avian influenza virus]
    J, > K[Identify primary or co-infecting agent]

Treatment

Antimicrobial therapy is the mainstay of treatment for turkey coryza. However, antimicrobial susceptibility patterns vary geographically, and resistance is common. Eldin et al. [10] reported high resistance rates to tetracycline, erythromycin, and sulfamethoxazole-trimethoprim among Egyptian isolates, while enrofloxacin and florfenicol retained efficacy. In vitro susceptibility testing should guide antibiotic selection. Administration of oxy-halogen formulations (e.g., stabilized chlorine dioxide) has been shown to improve poult performance following experimental challenge, likely due to direct bactericidal activity and reduction of environmental bacterial load [15]. Supportive care includes reducing stocking density, improving ventilation, and providing clean water and feed. Non-steroidal anti-inflammatory drugs may alleviate clinical signs.

Control and Prevention

Biosecurity is critical for preventing introduction and spread of B. avium. All-in/all-out management, thorough cleaning and disinfection between flocks, and strict visitor protocols reduce the risk of transmission. The bacterium is susceptible to common disinfectants, including quaternary ammonium compounds, chlorhexidine, and sodium hypochlorite.

Vaccination

Both live attenuated and inactivated vaccines have been evaluated. Hofstad and Jeska [16] demonstrated that intranasal administration of a live Artvax vaccine (a commercial live B. avium vaccine) and a formalin-inactivated bacterin induced protective immune responses in poults. Passive immunization via maternal antibodies has also been shown to protect poults against experimental challenge [17]. However, vaccination is not universally practiced due to variable efficacy and the risk of reversion to virulence with live vaccines. Autogenous bacterins may be used in flocks with persistent problems.

Flock Management

Early detection and isolation of affected birds, combined with antimicrobial treatment of in-contact birds, can limit the severity of outbreaks. Because B. avium infection predisposes turkeys to secondary bacterial infections (e.g., E. coli, ORT), comprehensive respiratory disease control programs should address all potential pathogens. Control of concurrent parasitic infections such as Spironucleus meleagridis and Cochlosoma anatis is also important to reduce overall disease burden.

References

[1] Jackwood MW, Sasser M, Saif YM. Contribution to the taxonomy of the turkey coryza agent: cellular fatty acid analysis of the bacterium. Avian Dis. 1986. URL: https://pubmed.ncbi.nlm.nih.gov/3729861/

[2] Jackwood MW, Saif YM, Moorhead PD, et al. Further characterization of the agent causing coryza in turkeys. Avian Dis. 1985. URL: https://pubmed.ncbi.nlm.nih.gov/4074238/

[3] Rimler RB, Rhoades KR. Turkey coryza: selected tests for detection and neutralization of Bordetella avium heat-labile toxin. Avian Dis. 1986. URL: https://pubmed.ncbi.nlm.nih.gov/3814017/

[4] Simmons DG, Dees C, Rose LP. A heat-stable toxin isolated from the turkey coryza agent, Bordetella avium. Avian Dis. 1986. URL: https://pubmed.ncbi.nlm.nih.gov/3814013/

[5] Rimler RB. Turkey coryza: toxin production by Bordetella avium. Avian Dis. 1985. URL: https://pubmed.ncbi.nlm.nih.gov/3833216/

[6] Simmons DG, Rose LP, Fuller FJ, et al. Turkey coryza: lack of correlation between plasmids and pathogenicity of Bordetella avium. Avian Dis. 1986. URL: https://pubmed.ncbi.nlm.nih.gov/3767817/

[7] Jackwood MW, Saif YM. Lack of protection against Bordetella avium in turkey poults exposed to B. avium-like bacteria. Avian Dis. 1987. URL: https://pubmed.ncbi.nlm.nih.gov/3675427/

[8] Śmiałek M, Tykałowski B, Pestka D, et al. Epidemiological situation of turkey coryza (bordetellosis) in Poland. Pol J Vet Sci. 2015. URL: https://pubmed.ncbi.nlm.nih.gov/26618601/

[9] Ehsan M, Hassanzadeh M, Barrin A, et al. A Study on Isolation and Molecular Identification of Bordetella avium from Iranian Commercial and Backyard Broiler Turkeys within 2016-2018. Arch Razi Inst. 2020. URL: https://pubmed.ncbi.nlm.nih.gov/32621446/

[10] Eldin WFS, Abd-El Samie LK, Darwish WS, et al. Prevalence, virulence attributes, and antibiogram of Bordetella avium isolated from turkeys in Egypt. Trop Anim Health Prod. 2020. URL: https://pubmed.ncbi.nlm.nih.gov/31376060/

[11] Kelly BJ, Ghazikhanian GY, Mayeda B. Clinical outbreak of Bordetella avium infection in two turkey breeder flocks. Avian Dis. 1986. URL: https://pubmed.ncbi.nlm.nih.gov/3729868/

[12] Yersin AG, Edens FW, Simmons DG. Effect of Bordetella avium infection on electrocardiograms in turkey poults. Avian Dis. 1991. URL: https://pubmed.ncbi.nlm.nih.gov/1785997/

[13] Hashish A, Sinha A, Mekky A, et al. Development and Validation of Two Diagnostic Real-Time PCR (TaqMan) Assays for the Detection of Bordetella avium from Clinical Samples and Comparison to the Currently Available Real-Time TaqMan PCR Assay. Microorganisms. 2021. URL: https://pubmed.ncbi.nlm.nih.gov/34835358/

[14] Register KB, Yersin AG. Analytical verification of a PCR assay for identification of Bordetella avium. J Clin Microbiol. 2005. URL: https://pubmed.ncbi.nlm.nih.gov/16272488/

[15] Pardue SL, Luginbuhl GH. Improvement of poult performance following Bordetella avium challenge by administration of a novel oxy-halogen formulation. Avian Dis. 1998. URL: https://pubmed.ncbi.nlm.nih.gov/9533091/

[16] Hofstad MS, Jeska EL. Immune response of poults following intranasal inoculation with Artvax vaccine and a formalin-inactivated Bordetella avium bacterin. Avian Dis. 1985. URL: https://pubmed.ncbi.nlm.nih.gov/4074243/

[17] Rimler RB, Kunkle RA. Passive immune protection of turkeys against Coryza. Avian Dis. 1997. URL: https://pubmed.ncbi.nlm.nih.gov/9454930/