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Bordetella holmesii: Comparison of Two Isolates from Blood and a Respiratory Sample

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DOI: 10.4236/aid.2013.32020    4,214 Downloads   6,486 Views   Citations

ABSTRACT

Interest in Bordetella holmesii is increasing, but very little is known about this bacterium, which can be isolated from both blood and respiratory samples. In this study, we compared a B. holmesii isolate from the blood sample of an adult with bacteremia with another isolate from a nasopharyngeal swab from an adult with whooping cough syndrome. Genetic analysis was carried out, targeting relevant genes, and virulence properties were studied in cellular and animal models. Our genomic analysis provided no evidence of traits specific to either blood or respiratory isolates of B. holmesii. Neither isolate was cytotoxic to human tracheal epithelial cells. Both isolates were only weakly invasive and they did not persist within epithelial cells for less than 48 h.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

V. Bouchez and N. Guiso, "Bordetella holmesii: Comparison of Two Isolates from Blood and a Respiratory Sample," Advances in Infectious Diseases, Vol. 3 No. 2, 2013, pp. 123-133. doi: 10.4236/aid.2013.32020.

References

[1] R. S. Weyant, D. G. Hollis, R. E. Weaver, M. F. M. Amin, A. G. Steigerwalt, S. P. O’Connor, A. M. Whitney, M. I. Daneshvar, C. W. Moss and D. J. Brenner, “Bordetella holmesii sp. nov., a New Gram-Negative Species Associated with Septicemia,” Journal of Clinical Microbiology, Vol. 33, No. 1, 1995, pp. 1-7.
[2] D. A. Diavatopoulos, C. A. Cummings, H. G. van der Heide, M. van Gent, S. Liew, D. A. Relman and F. R. Mooi, “Characterization of a Highly Conserved Island in the Otherwise Divergent Bordetella holmesii and Bordetella pertussis Genomes,” Journal of bacteriology, Vol. 188, No. 24, 2006, pp. 8385-8394. doi:10.1128/JB.01081-06
[3] G. Gerlach, S. Janzen, D. Beier and R. Gross, “Functional Characterization of the bvgAS Two-Component System of Bordetella holmesii,” Microbiology, Vol. 150, No. 11, 2004, pp. 3715-3729. doi:10.1099/mic.0.27432-0
[4] A. Horvat and R. Gross, “Molecular Characterization of the BvgA Response Regulator of Bordetella holmesii,” Microbiology Research, Vol. 164, No. 3, 2009, pp. 243-252. doi:10.1016/j.micres.2006.11.015
[5] S. Link, K. Schmitt, D. Beier and R. Gross, “Identification and regulation of expression of a gene encoding a filamentous hemagglutinin-related protein in Bordetella holmesii,” BMC Microbiology, Vol. 7, No. 2007, p. 100.
[6] A. Tizolova, N. Guiso and S. Guillot, “Insertion Sequences Shared by Bordetella Species and Implications for the Biological Diagnosis of Pertussis Syndrome,” European Journal of Clinical Microbiology Infectious Diseases, Vol. 32, No. 1, 2013, pp. 89-96. doi:10.1007/s10096-012-1718-3
[7] O. Vielemeyer, J. Y. Crouch, S. C. Edberg and J. G. Howe, “Identification of Bordetella pertussis in a Critically Ill Human Immunodeficiency Virus-Infected Patient by Direct Genotypical Analysis of Gram-Stained Material and Discrimination from B. holmesii by Using a Unique recA Gene Restriction Enzyme Site,” Journal of Clinical Microbiology, Vol. 42, No. 2, 2004, pp. 847-849. doi:10.1128/JCM.42.2.847-849.2004
[8] M. Antila, Q. He, C. de Jong, I. Aarts, H. Verbakel, S. Bruisten, S. Keller, M. Haanpera, J. Makinen, E. Eerola, M. K. Viljanen, J. Mertsola and A. van der Zee, “Bordetella holmesii DNA Is Not Detected in Nasopharyngeal Swabs from Finnish and Dutch Patients with Suspected Pertussis,” Journal of Medical Microbiology, Vol. 55, No. 8, 2006, pp. 1043-1051. doi:10.1099/jmm.0.46331-0
[9] J. L. Guthrie, A. V. Robertson, P. Tang, F. Jamieson and S. J. Drews, “Novel Duplex Real-Time PCR Assay Detects Bordetella holmesii in Specimens from Patients with Pertussis-Like Symptoms in Ontario, Canada,” Journal of Clinical Microbiology, Vol. 48, No. 4, 2010, pp. 1435-1437. doi:10.1128/JCM.02417-09
[10] L. Rodgers, S. W. Martin, A. Cohn, J. Budd, M. Marcon, A. Terranella, S. Mandal, D. Salamon, A. Leber, M. L. Tondella, K. Tatti, K. Spicer, A. Emanuel, E. Koch, L. McGlone, L. Pawloski, M. Lemaile-Williams, N. Tucker, R. Iyer, T. A. Clark and M. Diorio, “Epidemiologic and Laboratory Features of a Large Outbreak of Pertussis-Like Illnesses Associated with Co-Circulating Bordetella holmesii and Bordetella pertussis—Ohio, 2010-2011,” Clinical Infectious Diseases, Vol. 56, No. 3, 2013, pp. 322-331. doi:10.1093/cid/cis888
[11] F. R. Mooi, S. Bruisten, I. Linde, F. Reubsaet, K. Heuvelman, S. van der Lee and J. K. A, “Characterization of Bordetella holmesii Isolates from Patients with Pertussis-Like Illness in the Netherlands,” FEMS Immunology and Medical Microbiology, Vol. 64, No. 2, 2012, pp. 289-291. doi:10.1111/j.1574-695X.2011.00911.x
[12] S. Jonckheere, T. De Baere, P. Schroeyers, O. Soetens, A. De Bel and I. Surmont, “Prosthetic Valve Endocarditis Caused by Bordetella holmesii, an Acinetobacter Look-Alike,” Journal of Medical Microbiology, Vol. 61, No. 6, 2012, pp. 874-877. doi:10.1099/jmm.0.038695-0
[13] H. Kamiya, N. Otsuka, Y. Ando, F. Odaira, S. Yoshino, K. Kawano, H. Takahashi, T. Nishida, Y. Hidaka, H. Toyoizumi-Ajisaka, K. Shibayama, K. Kamachi, T. Sunagawa, K. Taniguchi and N. Okabe, “Transmission of Bordetella holmesii during Pertussis Outbreak, Japan,” Emerging Infectious Diseases, Vol. 18, No. 7, 2012, pp. 1166-1169. doi:10.3201/eid1807.120130
[14] D. M. Livovsky, D. Leibowitz, C. Hidalgo-Grass, V. Temper, S. Salameh and M. Korem, “Bordetella holmesii Meningitis in an Asplenic Patient with Systemic Lupus Erythematosus,” Journal of Medical Microbiology, Vol. 61, No. 8, 2012, pp. 1165-1167. doi:10.1099/jmm.0.038208-0
[15] E. Mazengia, E. A. Silva, J. A. Peppe, R. Timperi and H. George, “Recovery of Bordetella holmesii from Patients with Pertussis-Like Symptoms: Use of Pulsed-Field Gel Electrophoresis to Characterize Circulating Strains,” Journal of Clinical Microbiology, Vol. 38, No. 6, 2000, pp. 2330-2333.
[16] E. Njamkepo, S. Bonacorsi, M. Debruyne, S. A. Gibaud, S. Guillot and N. Guiso, “Significant Finding of Bordetella holmesii DNA in Nasopharyngeal Samples from French Patients with Suspected Pertussis,” Journal of Clinical Microbiology, Vol. 49, No. 12, 2011, pp. 4347-4348. doi:10.1128/JCM.01272-11
[17] W. K. Yih, E. A. Silva, J. Ida, N. Harrington, S. M. Lett and H. George, “Bordetella holmesii-Like Organisms Isolated from Massachussetts Patients with Pertussis-Like Symptoms,” Emerging Infectious Diseases, Vol. 5, No. 3, 1999, pp. 441-443. doi:10.3201/eid0503.990317
[18] X. Zhang, L. S. Weyrich, J. S. Lavine, A. T. Karanikas and E. T. Harvill, “Lack of Cross-Protection against Bordetella holmesii after Pertussis Vaccination,” Emerging Infectious Diseases, Vol. 18, No. 11, 2012, pp. 1771-1779.
[19] T. Chambaraud, Z. Dickson, G. Ensergueix, O. Barraud, M. Essig, C. Lacour, J. Allard, F. Bocquentin, J. C. Aldigier and J. P. Rerolle, “Bordetella holmesii Bacteremia in a Renal Transplant Recipient: Emergence of a New Pathogen,” Transplant Infectious Disease, Vol. 14, No. 6, 2012, pp. E134-E136. doi:10.1111/tid.12009
[20] M. I. Panagopoulos, M. Saint Jean, D. Brun, N. Guiso, S. Bekal, P. Ovetchkine and B. Tapiero, “Bordetella holmesii Bacteremia in Asplenic Children: Report of Four Cases Initially Misidentified as Acinetobacter lwoffii,” Journal of Clinical Microbiology, Vol. 48, No. 10, 2010, pp. 3762-3764. doi:10.1128/JCM.00595-10
[21] D. Bottero, M. M. Griffith, C. Lara, D. Flores, L. Pianciola, M. E. Gaillard, M. Mazzeo, M. I. Zamboni, M. J. Spoleti, E. Anchart, D. Ruggeri, C. Sorhouet, S. Fiori, M. Galas, M. L. Tondella and D. F. Hozbor, “Bordetella holmesii in Children Suspected of Pertussis in Argentina,” Epidemiology and infection, Vol. 141, No. 4, 2013, pp. 714-717. doi:10.1017/S095026881200132X
[22] C. Miranda, L. Porte and P. Garcia, “Bordetella holmesii in Nasopharyngeal Samples from Chilean Patients with Suspected Bordetella pertussis Infection,” Journal of Clinical Microbiology, Vol. 50, No. 4, 2012, p. 1505; Author Reply 1506.
[23] E. Njamkepo, F. Delisle, I. Hagege, G. Gerbaud and N. Guiso, “Bordetella holmesii Isolated from a Patient with Sickle Cell Anemia: Analysis and Comparison with Other Bordetella holmesii Isolates,” Clinical Microbiology and Infection, Vol. 6, No. 3, 2000, pp. 131-136. doi:10.1046/j.1469-0691.2000.00032.x
[24] V. Caro, E. Njamkepo, S. C. Van Amersfoorth, F. R. Mooi, A. Advani, H. O. Hallander, Q. He, J. Mertsola, M. Riffelmann, C. Vahrenholz, C. H. Von Konig and N. Guiso, “Pulsed-Field Gel Electrophoresis Analysis of Bordetella pertussis Populations in Various European Countries with Different Vaccine Policies,” Microbes Infection, Vol. 7, No. 7-8, 2005, pp. 976-982. doi:10.1016/j.micinf.2005.04.005
[25] C. Weber, C. Boursaux-Eude, G. Coralie, V. Caro and N. Guiso, “Polymorphism of Bordetella pertussis Isolates Circulating the Last Ten Years in France, Where a Single Effective Whole-Cell Vaccine Has Been Used for More Than Thirty Years,” Journal of Clinical Microbiology, Vol. 39, No. 12, 2001, pp. 4396-4403. doi:10.1128/JCM.39.12.4396-4403.2001
[26] V. Bouchez, D. Brun, T. Cantinelli, G. Dore, E. Njamkepo and N. Guiso, “First Report and Detailed Characterization of B. pertussis Isolates Not Expressing Pertussis Toxin or Pertactin,” Vaccine, Vol. 27, No. 43, 2009, pp. 6034-6041. doi:10.1016/j.vaccine.2009.07.074
[27] P. Software, “Phylogeny Inference Package (PHYLIP),” In: J. Felsenstein, Ed., PHYLIP—Phylogeny Inference Package (Version 3.2), Cladistics 5, Department of Genome Sciences, University of Washington, Seattle, 1989, pp. 164-166.
[28] N. Khelef and N. Guiso, “Induction of Macrophage Apoptosis by Bordetella pertussis Adenylate Cyclase-Hemolysin,” FEMS Microbiology Letters, Vol. 134, No. 1, 1995, pp. 27-32. doi:10.1111/j.1574-6968.1995.tb07909.x
[29] P. Gueirard, L. Bassinet, I. Bonne, M. C. Prevost and N. Guiso, “Ultrastructural Analysis of the Interactions between Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica and Human Tracheal Epithelial Cells,” Microbial pathogenesis, Vol. 38, No. 1, 2005, pp. 41-46. doi:10.1016/j.micpath.2004.08.003
[30] S. Mattoo, A. K. Foreman-Wykert, P. A. Cotter and J. F. Miller, “Mechanisms of Bordetella Pathogenesis,” Frontiers in Bioscience, Vol. 6, No. 86, 2001, p. 1.
[31] M. Sebaihia, 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, “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,” Journal of Bacteriology, Vol. 188, No. 16, 2006, pp. 6002-6015. doi:10.1128/JB.01927-05
[32] S. B. Loker, L. M. Temple and A. Preston, “The Bordetella avium BAV1965-1962 Fimbrial Locus Is Regulated by Temperature and Produces Fimbriae Involved in Adherence to Turkey Tracheal Tissue,” Infection and Immunity, Vol. 79, No. 6, 2011, pp. 2423-2429. doi:10.1128/IAI.01169-10
[33] A. Chahboune, M. Decaffmeyer, R. Brasseur and B. Joris, “Membrane Topology of the Escherichia coli AmpG Permease Required for Recycling of Cell Wall Anhydromuropeptides and AmpC Beta-Lactamase Induction,” Antimicrobial agents and chemotherapy, Vol. 49, No. 3, 2005, pp. 1145-1149. doi:10.1128/AAC.49.3.1145-1149.2005
[34] W. E. Goldman and B. T. Cookson, “Structure and Functions of the Bordetella Tracheal Cytotoxin,” The Tokai Journal of Experimental and Clinical Medicine, Vol. 13, 1988, pp. 187-191.
[35] K. M. Yen, M. R. Karl, L. M. Blatt, M. J. Simon, R. B. Winter, P. R. Fausset, H. S. Lu, A. A. Harcourt and K. K. Chen, “Cloning and Characterization of a Pseudomonas mendocina KR1 Gene Cluster Encoding Toluene-4-Monooxygenase,” Journal of Bacteriology, Vol. 173, No. 17, 1991, pp. 5315-5327.
[36] R. Gross, C. A. Guzman, M. Sebaihia, V. A. dos Santos, D. H. Pieper, R. Koebnik, M. Lechner, D. Bartels, J. Buhrmester, J. V. Choudhuri, T. Ebensen, L. Gaigalat, S. Herrmann, A. N. Khachane, C. Larisch, S. Link, B. Linke, F. Meyer, S. Mormann, D. Nakunst, C. Ruckert, S. Schneiker-Bekel, K. Schulze, F. J. Vorholter, T. Yevsa, J. T. Engle, W. E. Goldman, A. Puhler, U. B. Gobel, A. Goesmann, H. Blocker, O. Kaiser and R. Martinez-Arias, “The Missing Link: Bordetella petrii Is Endowed with Both the Metabolic Versatility of Environmental Bacteria and Virulence Traits of Pathogenic Bordetellae,” BMC Genomics, Vol. 9, 2008, p. 449.
[37] M. Lechner, K. Schmitt, S. Bauer, D. Hot, C. Hubans, E. Levillain, C. Locht, Y. Lemoine and R. Gross, “Genomic Island Excisions in Bordetella petrii,” BMC Microbiology, Vol. 9, 2009, p. 141.
[38] K. E. Stockbauer, A. K. Foreman-Wykert and J. F. Miller, “Bordetella Type III Secretion Induces Caspase 1-Independent Necrosis,” Cell Microbiology, Vol. 5, No. 2, 2003, pp. 123-132. doi:10.1046/j.1462-5822.2003.00260.x
[39] L. Bassinet, P. Gueirard, B. Maitre, B. Housset, P. Gounon and N. Guiso, “Role of Adhesins and Toxins in Invasion of Human Tracheal Epithelial Cells by Bordetella pertussis,” Infection and Immunity, Vol. 68, No. 4, 2000, pp. 1934-1941. doi:10.1128/IAI.68.4.1934-1941.2000
[40] Y. Ishibashi, D. A. Relman and A. Nishikawa, “Invasion of Human Respiratory Epithelial Cells by Bordetella pertussis: Possible Role for a Filamentous Hemagglutinin Arg-Gly-Asp Sequence and Alpha5beta1 Integrin,” Microbial Pathogenesis, Vol. 30, No. 5, 2001, pp. 279-288. doi:10.1006/mpat.2001.0432
[41] T. Spilker, A. A. Liwienski and J. J. LiPuma, “Identification of Bordetella spp. in Respiratory Specimens from Individuals with Cystic Fibrosis,” Clinical Microbiology Infection, Vol. 14, No. 5, 2008, pp. 504-506. doi:10.1111/j.1469-0691.2008.01968.x
[42] A. T. Harrington, J. A. Castellanos, T. M. Ziedalski, J. E. Clarridge 3rd and B. T. Cookson, “Isolation of Bordetella avium and Novel Bordetella Strain from Patients with Respiratory Disease,” Emerging Infectious Diseases, Vol. 15, No. 1, 2009, pp. 72-74. doi:10.3201/eid1501.0716

  
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