Chapter 43 : and Related Genera

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The genera , , , , and belong to the family Alcaligenaceae (order in the β subclass of the ). The genus was proposed for a set of strains phenotypically resembling that were classified as or as belonging to at least one other species. Virulence factors of bordetellae can be classified as adhesins, autotransporters (i.e., filamentous hemagglutinin [FHA], fimbriae [FIM], and pertactin [PRN]), and toxins (i.e., pertussis toxin [PT], adenylate cyclase toxin, and lipopolysaccharide [LPS]). For other bordetellae, normal microbiological transport media seem to be suitable for transport. Similarly, , , , and species can survive in a wide range of environments and at various temperatures. Commercial multiplex PCRs for the detection of various respiratory agents, including bordetellae, are available. Members of the genus can be separated from related species by their inability to assimilate phenyl acetate. and are susceptible in vitro to a range of antibiotics, including penicillins, macrolides, ketolides, quinolones, and other antibiotics, including tetracyclines, chloramphenicol, and trimethoprim-sulfamethoxazole, whereas they are resistant to most oral cephalosporins. Antimicrobial sensitivity testing of the isolates should be interpreted in accordance with criteria for other infrequently isolated and fastidious nonfermentative gram-negative rods.

Citation: Wirsing von König C, Riffelmann M, Coenye T. 2011. and Related Genera, p 739-750. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch43

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Bacterial Diseases
Restriction Fragment Length Polymorphism
Fourier Transform Infrared Spectroscopy
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Growth of on RL medium.

Citation: Wirsing von König C, Riffelmann M, Coenye T. 2011. and Related Genera, p 739-750. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch43
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1. Aisenberg, G.,, K. V. Rolston,, and A. Safdar. 2004. Bacteremia caused by Achromobacter and Alcaligenes species in 46 patients with cancer (1989-2003). Cancer 101:21342140.
2. Altunaiji, S.,, R. Kukuruzovic,, N. Curtis,, and J. Massie. 2. 2007. Antibiotics for whooping cough (pertussis). Cochrane Database Syst. Rev. 18:CD004404.
3. Antila, M.,, Q. He,, C. de Jong,, I. Aarts,, H. Verbakel,, S. Bruistenm,, S. Keller,, M. Haanperä,, J. Mäkinen,, E. Eerola,, M. J. Viljanen,, J. Mertsola,, and A. van der Zee. 2006. Bordetella holmesii DNA is not detected in nasopharyngeal swabs from Finnish and Dutch patients with suspected pertussis. J. Med. Microbiol. 55:10431051.
4. Arvand, M.,, R. Feldhues,, M. Mieth,, T. Kraus,, and P. Vandamme. 2004. Chronic cholangitis caused by Bordetella hinzii in a liver transplant recipient. J. Clin. Microbiol. 42:23352337.
5. Baughman, A. L.,, K. M. Bisgard,, K. M. Edwards,, D. Guris,, M. D. Decker,, K. Holland,, B. D. Meade,, and F. Lynn. 2004. Establishment of diagnostic cutoff points for levels of serum antibodies to pertussis toxin, filamentous hemagglutinin, and fimbriae in adolescents and adults in the United States. Clin. Diagn. Lab. Immunol. 11:10451053.
6. Bizet, J.,, and C. Bizet. 1997. Strains of Alcaligenes faecalis from clinical material. J. Infect. 35:167169.
7. Bizet, C.,, F. Tekaia,, and A. Philippon. 1993. In-vitro susceptibility of Alcaligenes faecalis compared with those of other Alcaligenes spp. to antimicrobial agents including seven betalactams. J. Antimicrob. Chemother. 32:907910.
8. Bordet, J.,, and U. Gengou. 1906. Le microbe de la coqueluche. Ann. Inst. Pasteur 20:4868.
9. Bosch, A.,, A. Miñán,, C. Vescina,, J. Degrossi,, B. Gatti,, P. Montanaro,, M. Messina,, M. Franco,, C. Vay,, J. Schmitt,, D. Naumann,, and O. Yantorno. 2008. Fourier transform infrared spectroscopy for rapid identification of nonfermenting gram-negative bacteria isolated from sputum samples from cystic fibrosis patients. J. Clin. Microbiol. 46:25352546.
10. Bosshard, P. P.,, R. Zbinden,, S. Abels,, B. Böddinghaus,, A. Altwegg,, and E. C. Böttger. 2006. 16S rRNA gene sequencing versus the API 20 NE system and the VITEK 2 ID-GNB card for identification of nonfermenting gram-negative bacteria in the clinical laboratory. J. Clin. Microbiol. 44:13591366.
11. Brinig, M. M.,, C. A. Cummings,, G. N. Sanden,, P. Stefanelli,, A. Lawrence,, and D. A. Relman. 2006. Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J. Bacteriol. 188:23752382.
12. Burns, J. L.,, J. Emerson,, J. R. Stapp,, D. L. Yim,, J. Krzewinski,, L. Louden,, B. W. Ramsey,, and C. R. Clausen. 1998. Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin. Infect. Dis. 27:158163.
13. Busse, H. J.,, and A. Stolz,. 2006. Achromobacter, Alcaligenes and related genera, p. 675700. In M. Dworkin,, S. Falkow,, E. Rosenberg,, K.-H. Schleifer,, and E. Stackebrandt (ed.), The Prokaryotes, vol. 5. Springer, Heidelberg, Germany.
14. Cagney, M.,, P. B. McIntyre,, L. Heron,, A. Giammanco,, and C. R. MacIntyre. 2008. The relationship between pertussis symptomatology, incidence and serology in adolescents. Vaccine 26:55475553.
15. Cattaneo, L. A.,, G. W. Reed,, D. H. Haase,, M. J. Wills,, and K. M. Edwards. 1996. The seroepidemiology of Bordetella pertussis infections: a study in persons ages 1-65 years. J. Infect. Dis. 173:12561259.
16.CDC. 2007. Outbreaks of respiratory illness mistakenly attributed to pertussis—New Hampshire, Massachusetts, and Tennessee, 2004-2006. Morb. Mortal Wkly. Rep. 56:837842.
17. Clarridge, J. E., III. 2004. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin. Microbiol. Rev. 17:840862.
18. Clermont, D.,, C. Harmant,, and C. J. Bizet. 2001. Identification of strains of Alcaligenes and Agrobacterium by a polyphasic approach. J. Clin. Microbiol. 39:31043109.
19. Coenye, T.,, J. Goris,, T. Spiker,, P. Vandamme,, and J. J. LiPuma. 2002. Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients, and description of Inquilinus limosus gen. nov. sp. nov. J. Clin. Microbiol. 40:20622069.
20. Coenye, T.,, M. Vancanneyt,, M. Cnockaert,, E. Falsen,, J. Swings,, and P. Vandamme. 2003. Kerstersia gyiorum gen. nov., sp. nov., a novel Alcaligenes faecalis-like organism isolated from human clinical samples, and reclassification of Alcaligenes denitrificans Rüger and Tan 1983 as Achromobacter denitrificans comb. nov. Int. J. Syst. Evol. Microbiol. 53:18251831.
21. Coenye, T.,, M. Vancanneyt,, E. Falsen,, J. Swings,, and P. Vandamme. 2003. Achromobacter insolitus sp. nov. and Achromobacter spanius sp. nov., from human clinical samples. Int. J. Syst. Evol. Microbiol. 53:18191824.
22. Coenye, T.,, E. Vanlaere,, E. Samyn,, E. Falsen,, and P. Vandamme. 2005. Advenella incenata gen. nov., sp. nov., a novel member of the Alcaligenaceae, isolated from various clinical samples. Int. J. Syst. Evol. Microbiol. 55:251256.
23. Cosnes-Lambe, C.,, J. Raymond,, M. Chalumeau,, C. Pons-Catalano,, F. Moulin,, N. de Suremain,, H. Reglier-Pupet,, P. Lebon,, C. Poyart,, and E. Grimprel. 2008. Pertussis and respiratory syncytial virus infections. Eur. J. Pediatr. 167:10171019.
24. Daxboeck, F.,, E. Goerzer,, P. Apfalter,, M. Nehr,, and R. Krause. 2004. Isolation of Bordetella trematum from a diabetic leg ulcer. Diabetes Med. 21:12471248.
25. De Baets, F.,, P. Schelstraete,, S. Van Daele,, F. Haerynck,, and M. Vaneechoutte. 2007. Achromobacter xylosoxidans in cystic fibrosis: prevalence and clinical relevance. J. Cyst. Fibros. 6:7578.
26. Degand, N.,, E. Carbonelle,, B. Dauphin,, J. L. Beretti,, M. Le Bourgeois,, I. Sermet-Gaudelus,, C. Segonds,, P. Berche,, X. Nassif,, and A. Ferroni. 2008. Matrix-assisted laser desorption ionization-time-of-flight mass spectrometry of nonfermenting gram-negative bacilli isolated from cystic fibrosis patients. J. Clin. Microbiol. 46:33613367.
27. De Melker, H. E.,, F. G. Versteegh,, M. A. Conyn-Van Spaendonck,, L. H. Elvers,, G. A. Berbers,, A. van der Zee,, and J. F. Schellekens. 2000.Specificity and sensitivity of high levels of immunoglobulin G antibodies to pertussis toxin in a single serum sample for diagnosis of infection with Bordetella pertussis. J. Clin. Microbiol. 38:800806.
28. Edwards, K. M.,, B. D. Meade,, M. D. Decker,, G. F. Reed,, M. B. Rennels,, M. C. Steinhoff,, E. L. Anderson,, J. A. Englund,, M. A. Pichichiero,, M. A. Deloria,, and A. Deforest. 1995. Comparison of 13 acellular pertussis vaccines: overview and serologic response. Pediatrics 96:548557.
29. Fenollar, F.,, V. Roux,, A. Stein,, M. Drancourt,, and D. Raoult. 2006. Analysis of 525 samples to determine the usefulness of PCR amplification and sequencing of the 16S rRNA gene for diagnosis of bone and joint infections. J. Clin. Microbiol. 44:10181028.
30. Fontana, C.,, M. Favaro,, M. Pellicioni,, E. S. Pistoia,, and C. Favalli. 2005. Use of the MicroSeq 500 16S rRNA gene-based sequencing for identification of bacterial isolates that commercial automated systems failed to identify. J. Clin. Microbiol. 43:615619.
31. Fry, N. K.,, O. Tzivra,, Y. T. Li,, A. Mcniff,, N. Doshi,, P. A. Maple,, N. S. Crowcroft,, E. Miller,, R. C. George,, and T. G. Harrison. 2004. Laboratory diagnosis of pertussis infections: the role of PCR and serology. J. Med. Microbiol. 53:519525.
32. Fry, N. K.,, J. Duncan,, H. Malnick,, M. Warner,, A. J. Smith,, M. S. Jackson,, and A. Ayoub. 2005. Bordetella petrii clinical isolate. Emerg. Infect. Dis. 11:11311133.
33. Fry, N. K.,, J. Duncan,, H. Malnick,, and P. M. Cockcroft. 2007. The first UK isolate of “ ansorpii” from an Bordetella immunocompromised patient. J. Med. Microbiol. 56:993995.
34. Fry, N. K.,, J. Duncan,, M. T. Edwards,, R. E. Tilley,, D. Chitvanis,, R. Harman,, H. Hammerton,, and L. Dalton. 2007. A UK clinical isolate of Bordetella hinzii from a patient with myelodysplastic syndrome. J. Med. Microbiol. 56:17001703.
35. Fry, N. K.,, J. Duncan,, K. Wagner,, O. Tzivra,, N. Doshi,, D. J. Litt,, N. Crowcroft,, E. Miller,, R. C. George,, and T. G. Harrison. 2009. Role of PCR in the diagnosis of pertussis infection in infants: 5 years’ experience of provision of a same-day real-time PCR service in England and Wales from 2002 to 2007. J. Med. Microbiol. 58:10231029.
36. Gerlach, G.,, S. Janzen,, D. Beier,, and R. Gross. 2004. Functional characterization of the BvgAS two-component system of Bordetella holmesii. Microbiology 150:37153729.
37. Giammanco, A.,, A. Nardone,, R. Pebody,, G. Kafatos,, N. Andrews,, A. Chiarini,, S. Taormina,, F. de Ory,, K. Prossenc,, B. Krize,, H. Hallander,, M. Ljungman,, E. Marva,, A. Tsakris,, D. O’Flanagan,, F. Schneider,, A. Griskevicius,, R. Vranckx,, and I. Karacs. 2008. European Sero-Epidemiology Network 2: standardization of immunoassay results for pertussis requires homogeneity of antigenic preparations. Vaccine 26:44864493.
38. Gibello, A.,, A. L. Vela,, M. Martin,, A. Barra-Caracciolo,, P. Grenni,, and J. F. Fernandez-Garayzabal. 2009. Reclassification of the members of the genus Tetrathiobacter Ghosh et al. 2005 to the genus Advenella Coenye et al. 2005. Int. J. Syst. Evol. Microbiol. 59:19141918.
39. Glupczynski, Y.,, W. Hansen,, J. Freney,, and E. Yourassowsky. 1988. In vitro susceptibility of Alcaligenes denitrificans subsp. xylosoxidans to 24 antimicrobial agents. Antimicrob. Agents Chemother. 32:276278.
40. Gómez-Cerezo, J.,, I. Suárez,, J. J. Ríos,, P. Peña,, M. J. García de Miguel,, M. de Joé,, O. Monteagudo,, P. Linares,, A. Barbado-Cano,, and J. J. Vázquez. 2003. Achromobacter xylosoxidans bacteremia: a 10-year analysis of 54 cases. Eur. J. Clin. Microbiol. Infect. Dis. 22:360363.
41. Gross, R.,, C. A. Guzman,, M. Sebaiihia,, V. A. P. Martins dos Santos,, D. H. Pieper,, R. Koebnik,, M. Lechner,, D. Bartels,, J. Buhrmeister,, J. V. Choudhouri,, T. Ebensen,, L. Gaigalat,, S. Hermann,, A. N. Khachane,, C. Larisch,, S. Link,, B. Linke,, F. Meyer,, S. Mormann,, D. Nakunst,, C. Rückert,, S. Schneikerbekel,, K. Schulze,, F. J. Vorhölter,, T. Yevsa,, J. T. Engle,, W. E. Goldman,, A. Pühler,, U. B. Göbel,, A. Goesmann,, H. Blöcker,, O. Kaiser,, and R. Martinez-Arias. 2008. The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic bordetellae. BMC Genomics 9:449.
42. Haberling, D. L.,, R. C. Holman,, C. D. Paddock,, and T. V. Murphy. 2009. Infant and maternal risk factors for pertussis-related infant mortality in the United States, 1999 to 2004. Pediatr. Infect. Dis. J. 28:194198.
43. Hallander, H. O.,, E. Reizenstein,, B. Renemar,, G. Rasmuson,, L. Mardin,, and P. Olin. 1993. Comparison of nasopharyngeal aspirates with swabs for culture of Bordetella pertussis. J. Clin. Microbiol. 31:5052.
44. Hallander, H.,, A. Advani,, M. Riffelmann,, C. H. Wirsing Von König,, V. Caro,, N. Guiso,, F. R. Mooi,, A. Gzyl,, M. S. Kaltoft,, N. K. Fry,, J. Mertsola,, and Q. He. 2007. Bordetella pertussis strain circulating in Europe in 1999 to 2004 as determined by pulsed field gel electrophoresis. J. Clin. Microbiol. 45:32573261.
45. Harrington, A. T.,, J. A. Castellanos,, T. M. Ziedalski,, J. E. Clarridge III,, and B. T. Cookson. 2009. Isolation of Bordetella avium and novel Bordetella strain from patients with respiratory disease. Emerg. Infect. Dis. 15:7274.
46. Henry, D. A.,, M. E. Campbell,, J. J. LiPuma,, and D. P. Speert. 1997. Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J. Clin. Microbiol. 35:614619.
47. Hewlett, E. L.,, G. M. Donato,, and M. C. Gray. 2006. Macrophage cytotoxicity produced by adenylate cyclase toxin from Bordetella pertussis: more than just making AMP. Mol. Microbiol. 59:447459.
48. Hijnen, M.,, Q. He,, R. Schepp,, P. van Gageldonk,, J. Mertsola,, F. R. Mooi,, and G. A. Berbers. 2008. Antibody responses to defined regions of the Bordetella pertussis virulence factor pertactin. Scand. J. Infect. Dis. 40:92104.
49. Hristov, A. C.,, P. G. Auwaerter,, M. Romagnoli,, and K. C. Caroll. 2008. Bordetella hinzii septicaemia in association with Epstein-Barr virus viremia and an Epstein-Barr virus-associated diffuse large B-cell lymphoma. Diagn. Microbiol. Infect. Dis. 61:484486.
50. Kadlec, K.,, J. Wiegand,, C. Kehrenberg,, and S. Schwarz. 2007. Studies on the mechanisms of beta-lactam resistance in Bordetella bronchiseptica. J. Antimicrob. Chemother. 59:396402.
51. Kanellopoulou, M.,, S. Pournaras,, H. Iglezos,, N. Skarmoutsou,, E. Papafrangas,, and A. N. Maniatis. 2004. Persistent colonization of nine cystic fibrosis patients with an Achromobacter (Alcaligenes) xylosoxidans clone. Eur. J. Clin. Microbiol. Infect. Dis. 23:336339.
52. Kattar, M. M.,, J. F. Chavez,, A. P. Limaye,, S. L. Rassoulianbarrett,, S. L. Yarfitz,, L. C. Carlson,, Y. Houze,, S. Swanzy,, B. L. Wood,, and B. T. Cookson. 2000. Application of 16S rRNA sequencing to identify Bordetella hinzii as the causative agent of fatal septicaemia. J. Clin. Microbiol. 38:789794.
53. Kay, S. E.,, R. A. Clark,, K. L. White,, and M. M. Peel. 2001. Recurrent Achromobacter piechaudii bacteremia in a patient with hematological malignancy. J. Clin. Microbiol. 39:808810.
54. Kersters, K.,, and J. De Ley,. 1984. Genus Alcaligenes Castellani and Chalmers 1919, 936AL, p. 361373. In N. R. Krieg, and J. G. Holt (ed.), Bergey’s Manual of Systematic Bacteriology, vol. 1. Williams & Wilkins Co., Baltimore, MD.
55. Kersters, K.,, K. H. Hinz,, A. Hertle,, P. Segers,, A. Lievens,, O. Siegmann,, and J. Deley. 1984. Bordetella avium sp. nov., isolated from the respiratory tracts of turkeys and other birds. Int. J. Syst. Bacteriol. 34:5670.
56. Kiredjian, M.,, B. Holmes,, K. Kersters,, I. Guilvout,, and J. De Ley. 1986. Alcaligenes piechaudii sp. nov., a new species from human clinical specimens and the environment. Int. J. Syst. Bacteriol. 36:282287.
57. Kiska, D. L.,, A. Kerr,, M. C. Jones,, J. A. Caracciolo,, B. Eskridge,, M. Jordan,, S. Miller,, D. Hughes,, N. King,, and P. H. Gilligan. 1996. Accuracy of four commercial systems for identification of Burkholderia cepacia and other gram-negative nonfermenting bacilli recovered from patients with cystic fibrosis. J. Clin. Microbiol. 34:886891.
58. Ko, K. S.,, K. R. Pecj,, W. S. Oh,, N. Y. Lee,, J. H. Lee,, and J. H. Song. 2005. New species of Bordetella, Bordetella ansorpii sp. nov., isolated from the purulent exudate of an epidermal cyst. J. Clin. Microbiol. 43:25162519.
59.Reference deleted.
60. Krzewinski, J. W.,, C. D. Nguyen,, J. M. Foster,, and J. L. burns. 2001. Use of random amplified polymorphic DNA PCR to examine epidemiology of Stenotrophomonas maltophilia and Achromobacter (Alcaligenes) xylosoxidans from patients with cystic fibrosis. J. Clin. Microbiol. 39:35973602.
61. Le, T.,, J. D. Cherry,, S. J. Chang,, M. D. Knoll,, M. L. Lee,, S. Barenkamp,, D. Bernstein,, R. Edelman,, K. M. Edwards,, D. Greenberg,, W. Keitel,, J. Treanor,, and J. I. Ward. 2004. Immune responses and antibody decay after immunization of adolescents and adults with an acellular pertussis vaccine: the APERT Study. J. Infect. Dis. 190:535544.
62. Liu, L.,, T. Coenye,, J. L. Burns,, P. W. Whitby,, T. L. Stull,, and J. J. Lipuma. 2002. rDNA-directed PCR for identification of Alcaligenes (Achromobacter) xylosoxidans recovered from cystic fibrosis sputum. J. Clin. Microbiol. 40:12101213.
63. Loeffelholz, M. J.,, C. J. Thompson,, K. S. Long,, and M. J. R. Gilchrist. 2000. Detection of Bordetella holmesii using Bordetella pertussis IS481 PCR assay. J. Clin. Microbiol. 38:467.
64. Lynn, F.,, G. F. Reed,, and B. D. Meade. 1996. Collaborative study for the evaluation of enzyme-linked immunosorbent assays used to measure human antibodies to Bordetella pertussis antigens. Clin. Diagn. Lab. Immunol. 3:689700.
65. Mackenzie, F. M.,, S. V. Smith,, K. E. Milne,, K. Griffiths,, J. Legge,, and I. M. Gould. 2004. Antibiograms of resistant gram-negative bacteria from Scottish CF patients. J. Cyst. Fibros. 3:151157.
66. Mattoo, S.,, and J. D. Cherry. 2005. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18:326382.
67. Mertens, P. L.,, F. S. Stals,, E. W. Steyerberg,, and J. H. Richardus. 2007. Sensitivity and specificity of single IgA and IgG antibody concentrations for early diagnosis of pertussis in adults: an evaluation for outbreak management in public health practice. BMC Infect. Dis. 7:53.
68. Moissenet, D.,, A. Baculard,, M. Valcin,, V. Marchand,, G. Tournier,, A. Garbarg-Chenon,, and H. Vu-Thien. 1997. Colonization by Alcaligenes xylosoxidans in children with cystic fibrosis: a retrospective clinical study conducted by means of molecular epidemiological investigation. Clin. Infect. Dis. 24:274275.
69. Moissenet, D.,, E. Bingen,, G. Arlet,, and H. Vu-Thien. 2005. Use of 16S rRNA gene sequencing for identification of Pseudomonas-like isolates from sputum of patients with cystic fibrosis. Pathol. Biol. (Paris) 53:500502.
70. Molina-Cabrillana, J.,, C. Santana-Reyes,, A. González-García,, A. Bordes-Benítez,, and I. Horcajada. 2007. Outbreak of Achromobacter xylosoxidans pseudobacteremia in a neonatal care unit related to contaminated chlorhexidine solution. Eur. J. Clin. Microbiol. Infect. Dis. 26:435437.
71. Moore, J. E.,, J. Xu,, b. C. Millar,, J. Courtney,, and J. S. Elborn. 2003. Development of a gram-negative selective agar (GNSA) for the detection of gram-negative microflora in sputa in patients with cystic fibrosis. J. Appl. Microbiol. 95:160166.
72. Mortensen, J. E.,, A. Brumbach,, and T. R. Shrycock. 1989. Antimicrobial susceptibility of Bordetella avium and Bordetella bronchiseptica isolates. Antimicrob. Agents Chemother. 33:771772.
73. Müller, F. M.,, J. E. Hoppe,, and, C. H. Wirsing von König. 1997. Diagnosis of pertussis: state of the art in 1997. J. Clin. Microbiol. 35:24352443.
74. Muyldermans, G.,, O. Soetens,, M. Antoine,, S. Bruisten,, B. Vincart,, K. Doucet,, F. Populaire,, N. K. Fry,, P. Olcen,, J. M. Scheftel,, J. M. Senterre,, A. van der Zee,, M. Riffelmann,, D. Pierard,, and S. Lauwers. 2005. External quality assessment for molecular detection of Bordetella pertussis in European laboratories. J. Clin. Microbiol. 43:3035.
75. Paddock, C. D.,, G. N. Sanden,, J. D. Cherry,, A. A. Gal,, C. Langston,, K. M. Tatti,, K. H. Wu,, C. S. Goldsmith,, P. W. Greer,, J. L. Montague,, M. T. Eliason,, R. C. Holman,, J. Guarner,, W. J. Shieh,, and S. R. Zaki. 2008. Pathology and pathogenesis of fatal Bordetella pertussis infections in infants. Clin. Infect. Dis. 47:328338.
76. Parkhill, J.,, M. Sebaihia,, A. Preston,, L. D. Murphy,, N. Thomson,, D. E. Harris,, M. T. Holden,, C. M. Churcher,, S. D. Bentley,, K. L. Mungall,, A. M. Cerdeño-Tárraga,, L. Temple,, K. James,, B. Harris,, M. A. Quail,, M. Achtman,, R. Atkin,, S. Baker,, D. Basham,, N. Bason,, I. Cherevach,, T. Chillingworth,, M. Collins,, A. Cronin,, P. Davis,, J. Doggett,, T. Feltwell,, A. Goble,, N. Hamlin,, H. Hauser,, S. Holroyd,, K. Jagels,, S. Leather,, S. Moule,, H. Norberczak,, S. O’Neil,, D. Ormond,, C. Price,, E. Rabbinowitsch,, S. Rutter,, M. Sanders,, D. Saunders,, K. Seeger,, S. Sharp,, M. Simmonds,, J. Skelton,, R. Squares,, S. Squares,, K. Stevens,, L. Unwin,, S. Whitehead,, B. G. Barrell,, And D. J. Maskell. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:3240.
77. Patriarca, P. A.,, R. J. Biellik,, G. Sanden,, D. G. Burstyn,, P. D. Mitchell,, P. R. Silverman,, J. P. Davis,, and C. R. Manclark. 1998. Sensitivity and specificity of clinical case definitions of pertussis. Am. J. Public Health 78:833836.
78. Pebody, R. G.,, N. J. Gay,, A. Giammanco,, S. Baron,, J. Schellekens,, A. Tischer,, R. M. Olander,, N. J. Andrews,, W. J. Edmunds,, H. Lecoeur,, D. Lévy-Bruhl,, P. A. Maple,, H. De Melker,, A. Nardone,, M. C. Rota,, S. Salmaso,, M. A. Conyn-van Spaendonck,, S. Swidsinski,, and E. Miller. 2005. The seroepidemiology of Bordetella pertussis infection in Western Europe. Epidemiol. Infect. 133:159171.
79. Plotkin, S. (ed.). 2005. The global pertussis initiative. Pediatr. Infect. Dis. J. 24:S5S98.
80. Raso, T.,, O. Bianco,, B. Grosso,, M. Zucca,, and D. Savoia. 2008. Achromobacter xylosoxidans respiratory tract infections in cystic fibrosis patients. APMIS 116:837841.
81. Rath, B. A.,, K. B. Register,, J. Wall,, D. M. Sokol,, and R. B. Van Dyke. 2008. Persistent Bordetella bronchiseptica pneumonia in an immunocompetent infant and genetic comparison of clinical isolates with kennel cough vaccine strains. Clin. Infect. Dis. 46:905908.
82. Register, K. B.,, R. E. Sacco,, and G. E. Nordholm. 2003. Comparison of ribotyping and restriction enzyme analysis for inter- and intraspecies discrimination of Bordetella avium and Bordetella hinzii. J. Clin. Microbiol. 41:15121519.
83. Register, K. B.,, and T. L. Nicholson. 2007. Misidentification of Bordetella bronchiseptica as Bordetella pertussis using a newly described real-time PCR targeting the pertactin gene. J. Med. Microbiol. 56:16081610.
84. Rehfuss, M.,, and J. Urban. 2005. Alcaligenes faecalis subsp. phenolicus subsp. nov. a phenol-degrading, denitrifying bacterium isolated from a graywater bioprocessor. Syst. Appl. Microbiol. 28:421429.
85. Reischl, U.,, N. Lehn,, G. N. Sanden,, and M. J. Loeffelholz. 2001. Real-time PCR assay targeting IS481 of Bordetella pertussis and molecular basis for detecting Bordetella holmesii. J. Clin. Microbiol. 39:19631966.
85a. Riffelmann, M.,, K. Thiel,, J. Schmetz,, and C. H. Wirsing von Koenig. 2010. Performance of commercial enzyme-linked immunosorbent assays for detection of antibodies to Bordetella pertussis. J. Clin. Microbiol. 48:44594463.
86. Riffelmann, M.,, C. H. Wirsing von König,, V. Caro,, and N. Guiso. 2005. Nucleic acid amplification tests for diagnosis of Bordetella infections. J. Clin. Microbiol. 43:49254929.
87. Rønne Hansen, C.,, T. Pressler,, N. Høiby,, and M. Gormsen. 2006. Chronic infection with Achromobacter xylosoxidans in cystic fibrosis patients; a retrospective case control study. J. Cyst. Fibros. 5:245251.
88. Saiman, L.,, Y. Chen,, P. San Gabriel,, and C. Knirsch. 2002. Synergistic activities of macrolide antibiotics against Pseudomonas aeruginosa, Burkholderia cepacia, Stenotrophomonas maltophilia, and Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. Antimicrob. Agents Chemother. 46:11051107.
89. Saiman, L.,, Y. Chen,, S. Tabibi,, P. San Gabriel,, J. Zhou,, Z. Liu,, L. Lai,, and S. Whittier. 2001. Identification and antimicrobial susceptibility of Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. J. Clin. Microbiol. 39:39423945.
90. Schroll, G.,, H. J. Busse,, G. Parrer,, S. Rölleke,, W. Lubitz,, and E. B. Denner. 2001. Alcaligenes faecalis subsp. parafaecalis subsp. nov., a bacterium accumulating poly-beta-hydroxybutyrate from acetone-butanol bioprocess residues. Syst. Appl. Microbiol. 24:3743.
91. Schwarz, S.,, E. Aleksik,, M. Grobbel,, A. Lübcke-Becker,, C. Werckenthin,, L. H. Wieler,, and J. Wallmann. 2007. Antimicrobial susceptibility of Pasteurella multocida and Bordetella bronchiseptica from dogs and cats as determined in the BfT-GermVet monitoring program 2004-2006. Berl. Munch. Tierarztl. Woschenschr. 120:423430.
92. Sebaihia, M.,, A. Preston,, D. J. Maskell,, H. Kuzmiak,, T. D. Connell,, N. D. King,, P. E. Orndorff,, D. M. Miyamoto,, N. R. Thomson,, D. Harris,, A. Goble,, A. Lord,, L. Murphy,, M. A. Quail,, S. Rutter,, R. Squares,, S. Squares,, J. Woodward,, J. Parkhill,, and L. M. Temple. 2006. Comparison of the genome sequence of the poultry pathogen Bordetella avium with those of B. bronchiseptica, B. pertussis and B. parapertussis reveals extensive diversity in surface structures associated with host interaction. J. Bacteriol. 188:60026015.
93. Shelly, D. B.,, T. Spilker,, E. J. Gracely,, T. Coenye,, P. Vandamme,, and J. J. LiPuma. 2000. Utility of commercial systems for identification of Burkholderia cepacia complex from cystic fibrosis sputum culture. J. Clin. Microbiol. 38:31123115.
94. Snyder, J. W.,, G. K. Munier,, and C. L. Johnson. 2008. Direct comparison of the BD Phoenix system with the MicroScan WalkAway system for identification and antimicrobial susceptibility testing of Enterobacteriaceae and nonfermentative gram-negative organisms. J. Clin. Microbiol. 46:23272333.
95. Spangler, S. K.,, M. A. Visalli,, M. R. Jacobs,, and P. C. Appelbaum. 1996. Susceptibilities of non-Pseudomonas aeruginosa gram-negative nonfermentative rods to ciprofloxacin, ofloxacin, levofloxacin, D-ofloxacin, sparfloxacin, ceftazidime, piperacillin, piperacillin-tazobactam, trimethoprim-sulfamethoxazole, and imipenem. Antimicrob. Agents Chemother. 40:772775.
96. Spicuzza, L.,, C. Sciuto,, G. Vitaliti,, G. Di Dio,, S. Leonardi,, and M. La Rosa. 2009. Emerging pathogens in cystic fibrosis: ten years of follow-up in a cohort of patients. Eur. J. Clin. Microbiol. Infect. Dis. 28:191195.
97. Spilker, T.,, A. A. Liwienski,, and J. J. LiPuma. 2008. Identification of Bordetella spp. in respiratory specimens from individuals with cystic fibrosis. Clin. Microbiol. Infect. 14:504506.
98. Stark, D.,, L. A. Riley,, J. Harkness,, and D. Mariott. 2007. Bordetella petrii from a clinical sample in Australia: isolation and molecular identification. J. Med. Microbiol. 56:435437.
99. Tatti, K. M.,, K. H. Wu,, M. L. Tondella,, P. K. Cassiday,, M. M. Cortese,, P. P. Wilkins,, and G. N. Sanden. 2008. Development and evaluation of dual-target real-time polymerase chain reaction assays to detect Bordetella spp. Diagn. Microbiol. Infect. Dis. 61:264272.
100. Templeton, K. E.,, S. A. Scheltinga,, A. van der Zee,, B. M. W. Diederen,, A. M. Kruijssen,, H. Goossens,, E. Kuijper,, and E. C. J. Claas. 2003. Evaluation of real-time PCR for detection of and discrimination between Bordetella pertussis, Bordetella parapertussis, and Bordetella holmesii for clinical diagnosis. J. Clin. Microbiol. 41:41214126.
101. Tondella, M. L.,, G. M. Carlone,, N. Messonnier,, C. P. Quinn,, B. D. Meade,, D. L. Burns,, J. D. Cherry,, N. Guiso,, E. L. Hewlett,, K. M. Edwards,, D. Xing,, A. Giammanco,, C. H. Wirsing von König,, L. Han,, L. Hueston,, J. B. Robbins,, M. Powell,, C. M. Mink,, J. T. Poolman,, S. W. Hildreth,, F. Lynn,, and A. Morris. 2009. International Bordetella pertussis assays standardization and harmonization meeting report. Vaccine 27:803814.
102. vanAmersfoorth, S. C. M.,, L. S. Schouls,, H. G. J. vanderHeide,, A. Advani,, H. O. Hallander,, K. Bondeson,, C. H. W. vonKönig,, M. Riffelmann,, C. Vahrenholz,, N. Guiso,, V. Caro,, E. Njamkepo,, Q. He,, J. Mertsola,, and F. R. Mooi. 2005. Analysis of Bordetella pertussis populations in European countries with different vaccine policies. J. Clin. Microbiol. 43:28372843.
103. VanDaele, S.,, R. Verhelst,, G. Claeys,, G. Verschraegen,, H. Franckx,, L. VanSimaey,, C. deGanck,, F. DeBaets,, and M. Vaneechoutte. 2005. Shared genotypes of Achromobacter xylosoxidans strains isolated from patients at a cystic fibrosis rehabilitation center. J. Clin. Microbiol. 43:29983002.
104. Vandamme, P.,, J. Hommez,, M. Vancanneyt,, M. Monsieurs,, B. Hoste,, B. Cookson,, C. H. Wirsing von Konig,, K. Kersters,, and P. J. Blackall. 1995. Bordetella hinzii sp. nov., isolated from poultry and humans. Int. J. Syst. Bacteriol. 45:3745.
105. Vandamme, P.,, M. Heyndrickx,, M. Vancanneyt,, B. Hoste,, P. DeVos,, E. Falsen,, K. Kersters,, and K. H. Hinz. 1996. Bordetella trematum sp. nov., isolated from wounds and ear infections in humans, and reassessment of Alcaligenes denitrificans Rüger and Tan 1983. Int. J. Syst. Bacteriol. 46:849858.
106. VanTrappen, S.,, T. L. Tan,, E. Samyn,, and P. Vandamme. 2005. Alcaligenes aquatilis sp. nov., a novel bacterium from sediments of the Weser Estuary, Germany, and a salt marsh on Shem Creek in Charleston Harbor, USA. Int. J. Syst. Evol. Microbiol. 55:25712575.
107. Versteegh, F. G.,, J. F. Schellekens,, A. F. Nagelkerke,, and J. J. Roord. 2002. Laboratory-confirmed reinfection with Bordetella pertussis. Acta Paediatr. 91:9597.
108. Versteegh, F. G.,, P. L. Mertens,, H. E. de Melker,, J. J. Roord,, J. F. Schellekens,, and P. F. Teunis. 2005. Agespecific long-term course of antibodies to pertussis toxin after symptomatic infection with Bordetella pertussis. Epidemiol. Infect. 133:737748.
109. Von Witzingerode, F.,, A. Schattke,, R. A. Siddiqui,, U. Rösick,, U. B. Göbel,, and R. Gross. 2001. Bordetella petrii sp. nov., isolated from an anaerobic bioreactor, and emended description of the genus Bordetella. Int. J. Syst. Evol. Microbiol. 51:12571265.
110. Wang, F.,, S. Grundmann,, M. Schmid,, U. Dörfler,, S. Roherer,, J. C. Munch,, A. Hartmann,, X. Jiang,, and R. Schroll. 2007. Isolation and characterization of 1,2,4-trichlorbenzene mineralizing Bordetella sp. and its bioremediation potential in soil. Chemosphere 76:896902.
111. Ward, J. I.,, J. D. Cherry,, S. J. Chang,, S. Partridge,, W. Keitel,, K. Edwards,, M. Lee,, J. Treanor,, D. P. Greenberg,, S. Barenkamp,, D. I. Bernstein,, R. Edelman, and the APERT Study Group. 2006. Bordetella pertussis infections in vaccinated and unvaccinated adolescents and adults as assessed in a national prospective randomized acellular pertussis vaccine trial (APERT). Clin. Infect. Dis. 43:151157.
112. Watanabe, M.,, B. Connelly,, and A. A. Weiss. 2006. Characterization of serological responses to pertussis. Clin. Vaccine Immunol. 13:341348.
113. Waters, V.,, F. Jamieson,, S. E. Richardson,, M. Finkelstein,, A. Wormsbecker,, and S. A. Halperin. 2009. Outbreak of atypical pertussis detected by polymerase chain reaction in immunized preschool-aged children. Pediatr. Infect. Dis. J. 28:582587.
114. Wellinghausen, N.,, B. Wirths,, and S. Poppert. 2006. Fluorescence in situ hybridization for rapid identification of Achromobacter xylosoxidans and Alcaligenes faecalis recovered from cystic fibrosis patients. J. Clin. Microbiol. 44:34153417.
115. Wendelboe, A. M.,, M. G. Hudgens,, C. Poole,, and A. van Rie. 2007. Estimating the role of casual contacts from the community in transmission of Bordetella pertussis to young infants. Emerg. Themes Epidemiol. 4:15.
116. Weyant, R. S.,, D. G. Hollis,, R. E. Weaver,, M. F. Amin,, A. G. Steigerwalt,, S. P. O’Connor,, A. M. Whitney,, M. I. Daneshvar,, C. W. Moss,, and D. J. Brenner. 1995. Bordetella holmesii sp. nov., a new gram-negative species associated with septicemia. J. Clin. Microbiol. 33:17.
117. Wirsing von König, C. H.,, S. Halperin,, M. Riffelmann,, and N. Guiso. 2002. Pertussis of adults and infants. Lancet Infect. Dis. 2:744750.
118. Wright, R. M.,, J. E. Moore,, A. Shaw,, K. Dunbar,, M. Dodd,, K. Webb,, A. O. Redmond,, M. Crowe,, P. G. Murphy,, S. Peacock,, and J. S. Elborn. 2001. Improved cultural detection of Burkholderia cepacia from sputum in patients with cystic fibrosis. J. Clin. Pathol. 54:803805.
119. Xing, D.,, C. H. Wirsing von König,, P. Newland,, M. Riffelmann,, B. D. Meade,, M. Corbel,, and R. Gaines-Das. 2009. Characterization of proposed reference materials for pertussis antiserum (human) by an international collaborative study. Clin. Vaccine Immunol. 16:303311.
120. Yabuuchi, E.,, Y. Kawamura,, Y. Kosako,, and T. Ezaki. 1998. Emendation of the genus Achromobacter and Achromobacter xylosoxidans (Yabuuchi and Yano) and proposal of Achromobacter ruhlandii (Packer and Vishniac) comb. nov., Achromobacter piechaudii (Kiredjian et al.) comb. nov., and Achromobacter xylosoxidans subsp. denitrificans (Rüger and Tan) comb. nov. Microbiol. Immunol. 42:429438.
121. Yih, W. K.,, S. M. Lett,, F. N. des Vignes,, K. M. Garrison,, P. L. Sipe,, and C. D. Marchant. 2000. The increasing incidence of pertussis in Massachusetts adolescents and adults, 1989-1998. J. Infect. Dis. 182:14091416.
122. Zbinden, A.,, E. C. Bötåtger,, P. P. Bosshard,, and R. Zbinden. 2007. Evaluation of the colorimetric VITEK 2 card for identification of gram-negative nonfermentative rods: comparison to 16S rRNA gene sequencing. J. Clin. Microbiol. 45:22702273.


Generic image for table
Table 1

Members of the genus

Citation: Wirsing von König C, Riffelmann M, Coenye T. 2011. and Related Genera, p 739-750. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch43
Generic image for table
Table 2

Biochemical reactions useful for differentiating and species

Data are from references , and .

Symbols and abbreviations: +, ≥90% of the strains are positive; –, ≤10% of the strains are positive; V, 10 to 89% of the strains are positive; ND, not determined.

Citation: Wirsing von König C, Riffelmann M, Coenye T. 2011. and Related Genera, p 739-750. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch43
Generic image for table
Table 3

Useful characteristics for differentiating species

Symbols and abbreviations: +, ≥90% of the strains are positive; –0, ≤10% of the strains are positive; V, 10 to 89% of the strains are positive; ND, not determined.

Citation: Wirsing von König C, Riffelmann M, Coenye T. 2011. and Related Genera, p 739-750. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch43

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