Ausschuss für Hygiene

Bordetella bronchiseptica

Host species:
  • laboratory animals (Goodnow 1980)
  • wide range of domestic and wild mammalian animals, birds, humans

Organotropism:
  • respiratory tract

Clinical disease:
  • many infected animals remain asymptomatic (Bemis 1992)
  • clinical disease is most commonly associated with respiratory symptoms such as sneezing, oculonasal discharge, coughing, and dyspnoe; signs of systemic disease include pyrexia, anorexia, chorioretinitis, vomiting, and diarrhea (Goodnow 1980, Harkness & Wagner 1995, Keil & Fenwick 1998, Speakman et al. 1999)
  • pig: atrophic rhinitis with resultant twisting or shortening of the snout; most severe disease in combination with toxigenic Pasteurella multocida infection (Kamp & Kimman 1988, Sakano et al. 1992)
  • dog: infectious tracheobronchitis (kennel cough) (Goodnow 1980, Keil & Fenwick 1998)
  • rabbit: snuffles; most infections become problematic only in association with Pasteurella multocida infection (Deeb et al. 1990)

Pathologys:
  • pig: rhinitis, atrophy of nasal turbinate bones, pneumonia (Goodnow 1980, Kamp & Kimman 1988, Sakano et al. 1992); ultrastructural changes in the turbinates are characterized by progressive degenerative changes in osteoblasts and osteocytes (Fetter et al. 1975, Silveira et al. 1982)
  • dog: rhinitis, sinusitis, tracheobronchitis, pneumonia (Goodnow 1980, Bemis 1992)
  • cat: tracheitis, suppurative bronchopneumonia, lymphadenitis (Speakman et al. 1999)
  • rabbit: serous to purulent rhinitis, catarrhal to purulent bronchopneumonia, pleuritis, hyperplasia of lymphoid tissues (Watson et al. 1972, Deeb et al. 1990, Glavits & Magyar 1990, Harkness & Wagner 1995)
  • guinea pig: serous to purulent otitis media, necrotizing tracheitis, suppurative necrotizing bronchopneumonia (Boot & Walfoort 1986, Trahan et al. 1987, Harkness & Wagner 1995)
  • rat: acute to subacute bronchopneumonia, atrophic rhinitis (Burek et al. 1972, Kimman & Kamp 1986)

Morbidity and mortality

  • differential host susceptibility: pigs, dogs, and guinea pigs are most susceptible; rats, rabbits, and horses have moderate susceptibility; chickens, mice, and humans are least susceptible (Goodnow 1980, Bemis 1992, Harkness & Wagner 1995)
  • B. bronchiseptica infection prevalence may vary from 0 to 100% depending on the population being tested; infections are generally higher in young animals, debiliated animals, and animals kept in close confinement
  • variation in the pathogenicity of B. bronchiseptica isolates
  • disease associated with B. bronchiseptica is frequently accompanied by infection with other agents
  • in general low mortality

Zoonotic relevance:
  • transmissible between species
  • airborne and contact transmission
  • infections in humans are often associated with an immunocompromised host (Woolfrey & Moody 1991)

Interference with research:

Physiology

  • lactic dehydrogenase activity and lactic acid and total protein concentrations were higher, and alkaline phosphatase acitivity was lower in blood plasma of severely affected pigs early in B. bronchiseptica infection compared with controls (Baetz et al. 1974)
  • neutral mucins are decreased in nasal mucosa of pigs infected with B. bronchiseptica (Perfumo et al. 1998)
  • in dogs, B. bronchiseptica infection leads to bronchial hyperresponsiveness to histamine (Dixon et al. 1979, Richards 1983) and methacholine (Nishikata et al. 1989); in guinea pigs, infection leads to hyperresponsiveness to histamine in the nasal mucosa with increased vascular permeability and recruitment of nociceptive nerve-parasympathetic reflexes (Gawin et al. 1998)
  • B. bronchiseptica dermonecrotizing toxin (DNT) impairs bone formation (Horiguchi et al. 1995a)

Cell biology

  • adherence of B. bronchiseptica to ciliated respiratory epithelial cells (Yokomizo & Shimizu 1979, Cotter et al. 1998) and induction of ciliostasis (Bemis & Wilson 1985)
  • evidence for binding of B. bronchiseptica to sialyl glycoconjugates on swine nasal mucosa (Ishikawa & Isayama 1987) and to glycosylated receptors on dendritic cells (Guzman et al. 1994a)
  • internalization and persistence of B. bronchiseptica in dendritic, epithelial, and phagocytic cells (Guzman et al. 1994b, Schipper et al. 1994, Forde et al. 1998)
  • B. bronchiseptica exerts a cytotoxic effect on various human cell lines (van den Akker 1997)
  • in osteoblast-like MC3T3-E1 cells, B. bronchiseptica DNT induces a morphological change, inhibits elevation of alkaline phosphatase activity, reduces accumulation of type I collagen (Horiguchi et al. 1991), stimulates DNA synthesis (Horiguchi et al. 1993) and protein synthesis (Horiguchi et al. 1994), induces membrane organelle proliferation and caveolae formation (Senda et al. 1997), and causes actin stress fiber formation and focal adhesions through the activation of the GTP-binding protein Rho (Horiguchi et al. 1995b, Horiguchi et al. 1997)
  • in Swiss 3T3 fibroblasts, Bordetella bronchiseptica DNT induces p21rho-dependent tyrosine phosphorylation of focal adhesion kinase and paxillin (Lacerda et al. 1997)

Immunology

  • alveolar macrophages from rabbits colonized with B. bronchiseptica exhibit ultrastructural and functional changes (alteration of metabolic activities upon stimulation, decreases in cell adherence, phagocytic uptake, and bactericidal activity) (Hoidal et al. 1978, Zeligs et al. 1986)
  • neutrophils are critical to the early defense against B. bronchiseptica infection (Harvill et al. 1999)
  • B. bronchiseptica induces primarily a Th1-type T-cell response (Gueirard et al. 1996)
  • serum concentrations of C-reactive protein are increased in dogs and monkeys infected with B. bronchiseptica (Yamamoto et al. 1994, Jinbo et al. 1999)
  • B. bronchiseptica DNT suppresses antibody responses in mice (Horiguchi et al. 1992)

Interactions with other infectious agents

  • B. bronchiseptica colonization may increase the severity of canine parainfluenza-2 virus in dogs (Wagener et al. 1984)
  • B. bronchiseptica infection predisposes the nasal mucosa to colonization with Pasteurella multocida in pigs (Chanter et al. 1989, Elias et al. 1992) and rabbits (Deeb et al. 1990, Harkness & Wagner 1995) enhanced adherence of Pasteurella multocida to porcine tracheal rings preinfected with Bordetella bronchiseptica (Dugal et al. 1992)

References:

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Bemis DA (1992) Bordetella and Mycoplasma respiratory infections in dogs and cats. Veterinary Clinics of North America: Small Animal Practice 22, 1173-86

Bemis DA, Wilson SA (1985) Influence of potential virulence determinants on Bordetella bronchiseptica-induced ciliostasis. Infection and Immunity 50, 35-42

Boot R, Walvoort HC (1986) Otitis media in guineapigs: pathology and bacteriology. Laboratory Animals 20, 242-8

Burek JD, Jersey GC, Whitehair CK, Carter GR (1972) The pathology and pathogenesis of Bordetella bronchiseptica and Pasteurella pneumotropica infection in conventional and germfree rats. Laboratory Animal Science 22, 844-9

Chanter N, Magyar T, Rutter JM (1989) Interactions between Bordetella bronchiseptica and toxigenic Pasteurella multocida in atrophic rhinitis of pigs. Research in Veterinary Science 47, 48-53

Cotter PA, Yuk MH, Mattoo S, Akerley BJ, Boschwitz J, Relman DA, Miller JF (1998) Filamentous hemagglutinin of Bordetella bronchiseptica is required for efficient establishment of tracheal colonization. Infection and Immunity 66, 5921-9

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Dixon M, Jackson DM, Richards IM (1979) The effect of a respiratory tract infection on histamine induced changes in lung mechanics and irritant receptor discharge in dogs. American Review of Respiratory Disease 120, 843-8

Dugal F, Belanger M, Jacques M (1992) Enhanced adherence of Pasteurella multocida to porcine tracheal rings preinfected with Bordetella bronchiseptica. Canadian Journal of Veterinary Research 56, 260-4

Elias B, Albert M, Tuboly S, Rafai P (1992) Interaction between Bordetella bronchiseptica and toxigenic Pasteurella multocida on the nasal mucosa of SPF piglets. Journal of Veterinary Medical Science 54, 1105-10

Fetter AW, Switzer WP, Capen CC (1975) Electron microscopic evaluation of bone cells in pigs with experimentally induced Bordetella rhinitis (turbinate osteoporosis). American Journal of Veterinary Research 36, 15-22

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Gueirard P, Minoprio P, Guiso N (1996) Intranasal inoculation of Bordetella bronchiseptica in mice induces long-lasting antibody and T-cell mediated immune responses. Scandinavian Journal of Immunology 43, 181-92

Guzman CA, Rohde M, Timmis KN (1994a) Mechanisms involved in uptake of Bordetella bronchiseptica by mouse dendritic cells. Infection and Immunity 62, 5538-44

Guzman CA, Rohde M, Timmis KN (1994b) Invasion and intracellular survival of Bordetella bronchiseptica in mouse dendritic cells. Infection and Immunity 62, 5528-37

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Harvill ET, Cotter PA, Yuk MH, Miller JF (1999) Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infection and Immunity 67, 1493-500

Hoidal JR, Beall GD, Rasp FL, Holmes B, White JG, Repine JE (1978) Comparison of the metabolism of alveolar macrophages from humans, rats, and rabbits: phorbol myristate acetate. Journal of Laboratory and Clinical Medicine 92, 787-94

Horiguchi Y, Inoue N, Masuda M, Kashimoto T, Katahira J, Sugimoto N, Matsuda M (1997) Bordetella bronchiseptica dermonecrotizing toxin induces reorganization of actin stress fibers through deamidation of Gln-63 of the GTP-binding protein Rho. Proceedings of the National Academy of Sciences of the United States of America 94, 11623-6

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Horiguchi Y, Nakai T, Kume K (1991) Effects of Bordetella bronchiseptica dermonecrotic toxin on the structure and function of osteoblastic clone MC3T3-E1 cells. Infection and Immunity 59, 1112-6

Horiguchi Y, Okada T, Sugimoto N, Morikawa Y, Katahira J, Matsuda M (1995a) Effects of Bordetella bronchiseptica dermonecrotizing toxin on bone formation in calvaria of neonatal rats. FEMS Immunology and Medical Microbiology 12, 29-32

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Horiguchi Y, Sugimoto N, Matsuda M (1993) Stimulation of DNA synthesis in osteoblast-like MC3T3-E1 cells by Bordetella bronchiseptica dermonecrotic toxin. Infection and Immunity 61, 3611-5

Horiguchi Y, Sugimoto N, Matsuda M (1994) Bordetella bronchiseptica dermonecrotizing toxin stimulates protein synthesis in an osteoblastic clone, MC3T3-E1 cells. FEMS Microbiology Letters 120, 19-22

Ishikawa H, Isayama Y (1987) Evidence for sialyl glycoconjugates as receptors for Bordetella bronchiseptica on swine nasal mucosa. Infection and Immunity 55, 1607-9

Jinbo T, Ami Y, Suzaki Y, Kobune F, Ro S, Naiki M, Iguchi K, Yamamoto S (1999) Concentrations of C-reactive protein in normal monkeys (Macaca irus) and in monkeys inoculated with Bordetella bronchiseptica R-5 and measles virus. Veterinary Research Communications 23, 265-74

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Kimman TG, Kamp EM (1986) Induced atrophic rhinitis in rats. American Journal of Veterinary Research 47, 2426-30

Lacerda HM, Pullinger GD, Lax AJ, Rozengurt E (1997) Cytotoxic necrotizing factor 1 from Escherichia coli and dermonecrotic toxin from Bordetella bronchiseptica induce p21rho-dependent tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 cells. Journal of Biological Chemistry 272, 9587-96

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Zeligs BJ, Zeligs JD, Bellanti JA (1986) Functional and ultrastructural changes in alveolar macrophages from rabbits colonized with Bordetella bronchiseptica. Infection and Immunity 53, 702-6
Author: M. Mähler