Genus Characteristics

Bordetella species are small (0.2–0.5 µm in diameter and 0.5–2.0 µm in length), Gram-negative rods which tend to be coccobacillary. They belong to the Alcaligenaceae family. The genus Bordetella accomodates currently eight species including the cause of pertussis or whooping cough in humans, B. pertussis. Three Bordetella species can be considered contagious respiratory pathogens in animals: B. bronchiseptica (porcine atrophic rhinitis; canine infectious tracheobronchitis, synonyms: kennel cough, canine cough, canine croup), B. avium (turkey coryza) and B. parapertussis (pneumonia in lambs).

Bordetella species are strict aerobes (except B. petrii) and do not ferment carbohydrates (asaccharolytic) but derive energy from the oxidation of amino and carboxylic acids. All are catalase-positive and oxidase-positive. Bordetella bronchiseptica and B. avium will grow on MacConkey agar. Bordetella avium and B. bronchiseptica are motile by peritrichous flagella, while B. pertussis and B. parapertussis are non-motile.

Natural Habitat

Bordetella species are contagious, obligatory parasites of the upper respiratory tract of healthy and diseased humans, animals and birds. Their distribution is worldwide. Bordetella bronchiseptica can be present as part of the flora of the upper respiratory tract of pigs, dogs, cats, rabbits, guinea-pigs, rats, horses and possibly other animals. The carrier rates for dogs, pigs and rabbits are reported to be high. Bordetella avium inhabits the respiratory tract of infected poultry, principally turkeys. Bordetella pertussis and B. parapertussis are human pathogens causing whooping cough and a mild form of whooping cough, respectively. Bordetella parapertussis has also been associated with a nonprogressive pneumonia in lambs.

Mammalian infections are mainly transmitted by aerosol via expired droplets. Infected animals represent the main sources of infection. In turkeys, indirect spread can occur via water and litter. The environmental survival capacity of Bordetella species is short and they are easily killed by UV radiation, pH, temperature and common disinfectants. However, B. avium and B. bronchiseptica are more resistant to various physical and chemical conditions than B. pertussis and B. parapertussis.

Pathogenicity and Pathogenesis

The bordetellae are associated with contagious respiratory diseases with high morbidities and low mortalities. Typical clinical signs include coughing with or without dyspnea, ocular or nasal discharge and weight loss. The severity of the disease increases with concomitant infection with other pathogenic respiratory agents. Table 28.1 summarizes the main diseases and hosts of Bordetella species. Bordetella bronchiseptica is the aetiological agent of infectious tracheobronchitis (kennel cough) in dogs and atrophic rhinitis in pigs. Respiratory infections associated with B. bronchiseptica have also been described in rabbits, cats, horses, rats, guinea pigs and less commonly in wildlife. Zoonotic diseases such as wound infections, bacteraemia and respiratory infections caused by B. bronchiseptica have been reported in the human literature but seem to be uncommon. Bordetella avium is the aetiological agent of turkey coryza or bordetellosis, a respiratory disease responsible for substantial economic losses in the poultry industry, especially in turkey production. This bacterium can also infect various species of fowl and songbirds (Raffel et al. 2002). Boredetella hinzii is generally regarded as non-pathogenic but some strains may be capable of causing disease in turkeys (Register & Kunkle 2009). Bordetella parapertussis is the cause of a nonprogressive form of pneumonia in lambs and a mild form of whooping cough in humans. Ovine and human strains of B. parapertussis are distinct with different host specificities.

Bordetella species virulence factors are summarized in Table 28.2. Virulence factors such as fimbriae (FIM), filamentous haemagglutinin (FHA), pertactin (PTN) and products of the type III secretion system promote adherence and colonization in Bordetella species. Virulence factors such as dermonecrotic toxin (DNT), osteotoxin, adenylate cyclase toxin (ACT), tracheal cytotoxin (TCT), pertussis toxin (PTX), type III secretion proteins and lipopolysaccharide (LPS) alter host tissues and promote lesion formation. Mattoo et al. (2001) reviewed the mechanisms of Bordetella pathogenesis.

Virulent strains of Bordetella species attach firmly to ciliated respiratory epithelium via attachment factors (FHA, FIM or PTN) and this is followed by rapid proliferation, ciliary paralysis and an inflammatory response. Bordetella species also have LPS which likely plays a role in colonization of the respiratory tract (Spears et al. 2000). Certain species of Bordetella produce an extracellular enzyme, adenylate cyclase haemolysin (ACT), which is a member of the RTX (Repeat in Toxins) family and has antiphagocytic activity. Dermonecrotic toxin (DNT) is a thermolabile intracellular polypeptide primarily responsible for nasal turbinate atrophy via alteration of osteoblast differentiation in B. bronchiseptica infections of pigs. It also produces necrotic lesions if injected intradermally. The effect on the turbinate bones is most serious in young pigs under three weeks of age when osteogenesis is most active. Atrophic rhinitis in pigs is transient and self-limiting when caused by B. bronchiseptica alone but the bacterium aids the establishment of the piliated and toxigenic strains of Pasteurella multocida and the combined infection causes more serious and permanent lesions (Fig. 28.1). Bordetella avium produces an osteotoxin which also alters osteoblast functions but without any dermonecrotic activity.

Bordetella species infections depress the respiratory clearance mechanisms facilitating invasion by other organisms. Both B. bronchiseptica and B. parapertussis have a type III secretion system (TTSS) which contributes to bacterial survival in the lower respiratory tract of the host (Pilione & Harvill 2006). The type III secretion products seem to be involved in cytotoxicity, apoptosis and inactivation of NF-κB (transcription factor) of eukaryotic cells. It is thought that persistent colonization by B. bronchiseptica may rely on the ability of the bacteria to differentially modulate both macrophage and dendritic cell functions leading to a modified adaptive immune response and subsequent bacterial colonization (Siciliano et al. 2006).

Bordetella species have genetic regulatory systems which contribute to pathogenesis of disease through modulation of virulence factors. Bordetella species utilize the BvgAS (Bordetella virulence gene) two-component signal transduction system to sense the environment and regulate gene expression with at least three phases: a virulent Bvg+ phase, a non-virulent Bvg– phase, and an intermediate Bvgi phase. Genes expressed in the Bvg+ phase encode virulence factors including adhesins (FHA and FIM) and toxins such as ACT. In the Bvgi phase, FHA and FIM continue to be expressed, however ACT expression is significantly downregulated. Bordetella bronchiseptica can form biofilms in vitro, the generation of biofilm is maximal in the Bvgi phase.

Laboratory Diagnosis