Bordetella bronchiseptica and Atrophic Rhinitis in Pigs: Turbinate Atrophy and Diagnosis

Introduction

Atrophic rhinitis (AR) is a globally significant respiratory disease of swine characterized by progressive atrophy of the nasal turbinate bones, often leading to facial deformation, reduced growth performance, and increased susceptibility to secondary respiratory infections [1, 2]. The disease is a multifactorial syndrome primarily initiated by Bordetella bronchiseptica, a Gram-negative coccobacillus, and exacerbated by toxigenic strains of Pasteurella multocida [3, 4]. The economic impact of AR stems from decreased feed conversion efficiency, increased carcass condemnation, and the costs associated with vaccination and antimicrobial therapy [2, 5].

B. bronchiseptica acts as a primary colonizer of the porcine upper respiratory tract, adhering to ciliated nasal epithelium and producing virulence factors that damage the mucosal barrier and suppress local immune responses [1, 5]. The hallmark of AR is the loss of nasal turbinate structure, a direct consequence of osteoclastic resorption triggered by bacterial dermonecrotic toxin (DNT) and, in synergistic infections, P. multocida toxin (PMT) [3, 6]. This article provides a comprehensive review of the pathophysiological mechanisms of turbinate atrophy, diagnostic methodologies including imaging and molecular assays, and control strategies based on the experimental literature.

Etiology and Pathogenesis

Bordetella bronchiseptica is a small, aerobic, motile, Gram-negative rod that belongs to the genus Bordetella [1]. It is a common commensal and pathogen of the respiratory tract in swine, capable of persistent colonization [1, 5]. The organism expresses multiple adhesins, including filamentous hemagglutinin (FHA), pertactin, and fimbriae, which mediate attachment to ciliated epithelial cells in the nasal cavity [5]. Following adherence, B. bronchiseptica produces a suite of toxins, the most relevant being the dermonecrotic toxin (DNT), a heat-labile protein that acts as a potent stimulator of osteoclastic bone resorption [3, 5].

Experimental infection models have demonstrated that B. bronchiseptica alone can induce mild to moderate turbinate atrophy in gnotobiotic and conventionally reared piglets [7, 8]. In studies using sequential infection, piglets inoculated with B. bronchiseptica followed by toxigenic P. multocida developed severe, progressive atrophy that mirrored naturally occurring progressive atrophic rhinitis (PAR) [7, 8, 9]. The initial B. bronchiseptica infection is thought to damage the nasal epithelium, thereby facilitating colonization and toxin delivery by P. multocida [10]. The ability of B. bronchiseptica to predispose to P. multocida infection does not strictly require DNT expression, as demonstrated by Brockmeier and Register [4], who showed that DNT-negative B. bronchiseptica mutants still enhance subsequent P. multocida colonization. This finding indicates that other virulence factors of B. bronchiseptica contribute to mucosal disruption.

Transmission of B. bronchiseptica occurs via direct contact with respiratory secretions and through aerosolized droplets [1]. A vertical transmission model has been established, demonstrating that sows can transmit the organism to their offspring during the perinatal period, leading to early colonization of piglets [1]. This early exposure is critical because the severity of AR is inversely correlated with the age at initial infection; younger piglets develop more pronounced turbinate atrophy [7, 11].

Toxins and Mechanisms of Turbinate Atrophy

Dermonecrotic Toxin (DNT) of Bordetella bronchiseptica

DNT is a 145 kDa protein that is the primary virulence factor of B. bronchiseptica responsible for turbinate destruction [3, 5]. The toxin acts via transglutaminase activity, deamidating or polyaminating specific glutamine residues in small GTPases such as RhoA, Rac1, and Cdc42 [3]. This constitutive activation of Rho GTPases leads to increased osteoclast differentiation and activity, resulting in net bone resorption [3]. In the nasal turbinates, DNT stimulates osteoclastogenesis both directly and indirectly through upregulation of receptor activator of nuclear factor-kappa B ligand (RANKL) on osteoblasts [3].

The effects of DNT are not limited to bone; the toxin also induces necrosis of soft tissues, particularly in the skin when injected intradermally, hence the name dermonecrotic toxin [3, 5]. In the respiratory tract, DNT causes epithelial cell necrosis, ciliostasis, and submucosal inflammation, which collectively impair mucociliary clearance and promote bacterial persistence [5].

Pasteurella multocida Toxin (PMT)

Toxigenic strains of P. multocida serotype D and occasionally serotype A produce PMT, a 146 kDa protein that is the primary driver of severe, progressive AR [3, 10, 12]. PMT is a potent mitogen and inducer of osteoclast activation, with a mechanism distinct from DNT. PMT activates heterotrimeric G proteins of the Gq/11 and Gi families, leading to phospholipase C activation, calcium mobilization, and downstream signaling through protein kinase C and Ras [3]. The result is profound stimulation of bone resorption, leading to complete loss of nasal turbinates in experimentally infected pigs [7, 8, 10].

The synergistic action of DNT and PMT is responsible for the most severe forms of AR. Chanter et al. [10] demonstrated that sequential infection with B. bronchiseptica followed by toxigenic P. multocida produced significantly more severe atrophy than either agent alone. Sakano et al. [7] confirmed that older pigs (2 and 4 months of age) also develop substantial atrophy after sequential infection, although lesions were less severe than in younger piglets.

Interactions between Bordetella bronchiseptica and Pasteurella multocida

The relationship between B. bronchiseptica and P. multocida in AR is cooperative and synergistic. B. bronchiseptica is not merely a primary pathogen but also a facilitator for the establishment of P. multocida [4, 10]. The mechanisms by which B. bronchiseptica predisposes to P. multocida colonization include:

• Damage to the ciliated epithelium, removing physical barriers [5].
• Production of a biofilm or extracellular matrix that provides adhesion sites for P. multocida [4].
• Suppression of local host immunity, including inhibition of phagocytosis and modulation of cytokine responses [5].

Brockmeier and Register [4] showed that a DNT-deficient mutant of B. bronchiseptica retained the ability to enhance P. multocida colonization, indicating that other factors such as filamentous hemagglutinin or tracheal cytotoxin may be critical for this synergistic interaction. The presence of both organisms correlates with more severe turbinate atrophy and a higher likelihood of clinical AR in field settings [2, 11].

Clinical Signs and Gross Lesions

Clinical signs of AR are most commonly observed in growing pigs between 3 and 8 weeks of age [2, 9]. The earliest sign is sneezing, often accompanied by serous to mucopurulent nasal discharge [2, 5]. As turbinate atrophy progresses, distortion of the nasal bone may become visible externally, manifesting as shortening or twisting of the snout [2, 9]. In severe cases, the pig may exhibit epistaxis and increased tearing due to obstruction of the nasolacrimal duct [5].

The gross pathological hallmark of AR is atrophy of the ventral and dorsal nasal conchae, most pronounced in the ventral scrolls [9]. Martineau-Doizé et al. [9] described the distribution of atrophy in experimentally infected piglets, noting that the rostral portion of the ventral conchae is typically affected first, progressing caudally. Scoring systems for turbinate atrophy, such as the method described by Baalsrud [13], rely on cross-sectioning the snout at the level of the first premolar tooth and grading the degree of conchal loss on a 0 to 4 scale.

Systemic effects include reduced average daily weight gain and feed efficiency, as documented by Bäckström et al. [11] in long-term exposure studies. These production losses occur even in the absence of overt clinical signs, making subclinical AR an important economic constraint.

Diagnosis

Clinical and Gross Examination

The initial diagnosis of AR is often based on clinical signs and snout morphology. However, subclinical cases require postmortem examination of the nasal cavity [2, 9]. The classic diagnostic procedure involves sawing the snout transversely at the level of the first premolar tooth and visually assessing turbinate integrity. Scoring systems allow semiquantitative evaluation of atrophy [13].

Imaging and Automated Assessment

Advanced imaging techniques have been developed to quantify turbinate atrophy more objectively. Lichterfeld et al. [2] described an automatic imaging method that uses digital image analysis of snout cross-sections to calculate the ratio of turbinate bone area to total nasal cavity area. This technique reduces interobserver variability and provides continuous data suitable for statistical analyses [2].

Bacteriological Culture and Isolation

Isolation of B. bronchiseptica from nasal swabs or tissue homogenates remains a standard diagnostic approach. The organism grows on selective media such as MacConkey agar and Bordet-Gengou agar, producing characteristic small, smooth, hemolytic colonies after 24 to 48 hours of aerobic incubation [5]. Identification is confirmed by Gram stain morphology, oxidase and urease positivity, and motility [5]. However, culture may be insensitive in chronically infected or antibiotic-treated animals [2].

Molecular Detection

Polymerase chain reaction (PCR) assays targeting the fla gene or the DNT gene (dnt) of B. bronchiseptica provide high sensitivity and specificity [2]. Multiplex PCR panels that simultaneously detect B. bronchiseptica, P. multocida, and other respiratory pathogens (e.g., Mycoplasma hyopneumoniae, influenza A virus) are increasingly used for herd-level diagnosis [2]. Quantitative real-time PCR (qPCR) allows bacterial load estimation, which correlates with lesion severity [2].

Serological Assays

Commercial enzyme-linked immunosorbent assay (ELISA) kits for detection of antibodies against B. bronchiseptica are available. Serology is used primarily for herd monitoring and vaccine response assessment rather than individual diagnosis [13]. Antibodies against DNT and PMT can be measured to indicate exposure to toxigenic strains [3, 6].

Diagnostic Algorithm

The following Mermaid diagram summarizes a recommended diagnostic workflow for AR in swine.

flowchart TD
    A["Clinical suspicion: sneezing, nasal discharge, snout distortion"] --> B{Antemortem nasal swab}
    B --> C["PCR panel: B. bronchiseptica, P. multocida, other pathogens"]
    C --> D[Positive for B. bronchiseptica?]
    D -->|Yes| E[Quantify bacterial load by qPCR]
    D -->|No| F[Consider other respiratory diseases]
    E --> G[Postmortem snout cross-section at first premolar]
    G --> H[Gross scoring or automated imaging]
    H --> I[Calculate turbinate atrophy index]
    I --> J{Atrophy score > 1?}
    J -->|Yes| K[Confirm AR diagnosis]
    J -->|No| L["Subclinical colonization; monitor herd"]
    K --> M["Toxin typing: DNT PCR / PMT ELISA"]
    M --> N[Institute vaccination and management changes]

Differential Diagnosis

The clinical presentation of AR must be differentiated from other causes of nasal discharge and sneezing in pigs, including infection with Mycoplasma hyorhinis, influenza A virus, porcine reproductive and respiratory syndrome virus, and environmental irritants (e.g., ammonia, dust) [2]. Turbinate atrophy is not seen in these conditions. Concurrent infection with P. multocida should be confirmed by culture and/or PCR to establish the risk of severe PAR [7, 10].

Vaccination and Control

Vaccination is a cornerstone of AR control in commercial herds. Both bacterins (whole-cell inactivated B. bronchiseptica) and toxoid vaccines targeting DNT and PMT are available [6, 14, 13]. Sakano et al. [6] demonstrated that a combined B. bronchiseptica bacterin and P. multocida toxoid significantly reduced the incidence and severity of AR in experimentally infected pigs. Kobisch and Pennings [14] reported similar efficacy with a vaccine containing PMT toxoid and B. bronchiseptica antigens.

Vaccination of sows before farrowing provides passive immunity to piglets via colostrum, delaying or preventing early colonization [1]. Vertical transmission models underscore the importance of sow vaccination, as piglets born to vaccinated sows have lower nasal colonization rates and reduced turbinate atrophy [1, 13].

Antimicrobial therapy, while used, is often of limited efficacy due to biofilm formation and the intracellular niche of B. bronchiseptica [5]. Management practices such as all-in/all-out production, improved ventilation, and reduced stocking density help reduce bacterial load and clinical expression of AR [11].

Summary

Bordetella bronchiseptica is a primary etiological agent of atrophic rhinitis in swine, inducing turbinate atrophy through the action of dermonecrotic toxin and facilitating colonization by toxigenic Pasteurella multocida. The pathogenesis involves osteoclast activation, epithelial damage, and immune modulation. Diagnosis relies on clinical evaluation, postmortem imaging, culture, and molecular assays. Vaccination of sows with combined bacterin-toxoid preparations is the most effective control strategy. Continued research into vertical transmission and pathogen synergy will further refine diagnostic and preventive protocols.

References

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[2] Lichterfeld H, Trittmacher S, Gerdes K, et al. Porcine nose atrophy assessed by automatic imaging and detection of Bordetella bronchiseptica and other respiratory pathogens in lung and nose. Animals (Basel). 2024. URL: https://pubmed.ncbi.nlm.nih.gov/39518836/

[3] Horiguchi Y. Swine atrophic rhinitis caused by Pasteurella multocida toxin and Bordetella dermonecrotic toxin. Curr Top Microbiol Immunol. 2012. URL: https://pubmed.ncbi.nlm.nih.gov/22411430/

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[13] Baalsrud KJ. Vaccination against atrophic rhinitis: effect on clinical symptoms, growth rate and turbinate atrophy. Acta Vet Scand. 1987. URL: https://pubmed.ncbi.nlm.nih.gov/3454542/

[14] Kobisch M, Pennings A. An evaluation in pigs of Nobi-Vac AR and an experimental atrophic rhinitis vaccine containing P multocida DNT-toxoid and B bronchiseptica. Vet Rec. 1989. URL: https://pubmed.ncbi.nlm.nih.gov/2919495/ *** Disclaimer: This article is for educational and informational purposes only. It is not intended to substitute for professional veterinary advice, diagnosis, treatment, or regulatory guidance. Always consult a licensed veterinarian or qualified specialist regarding animal health, disease diagnosis, and therapeutic decisions.