Virulence phenotypes of low-passage clinical isolates of Nontypeable Haemophilus influenzae assessed using the chinchilla laniger model of otitis media

BMC Microbiology

Volumn 7, Issue , 2007, Pages

  Buchinsky, Farrel J ^a,b   Forbes, Michael L ^a   Hayes, Jay D ^a   Shen, Kai ^a   Ezzo, Suzanne ^a   Compliment, James ^a   Hogg, Justin ^a   Hiller, N Luisa ^a   Hu, Fen Ze ^b   Post, J Christopher ^a,b   Ehrlich, Garth D ^a,b  

^a ALLEGHENY GENERAL HOSPITAL   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CHINCHILLA; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DATA COLLECTION METHOD; DISEASE COURSE; DISEASE SEVERITY; HAEMOPHILUS INFLUENZAE; HUMAN; INOCULATION; MORTALITY; NONHUMAN; OTITIS MEDIA; OTORHINOLARYNGOLOGY; OTORRHEA; PARAMETER; PHENOTYPE; POST HOC ANALYSIS; SCORING SYSTEM; SYSTEMIC DISEASE; ANIMAL; BACTERIAL INFECTION; BACTERIUM IDENTIFICATION; CHILD; CLASSIFICATION; CLUSTER ANALYSIS; DISEASE MODEL; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; PATHOPHYSIOLOGY; POLYMERASE CHAIN REACTION; SURVIVAL; TIME; VIRULENCE;

ANIMALIA; CHINCHILLA LANIGERA; HAEMOPHILUS INFLUENZAE;

ANIMALS; BACTERIAL TYPING TECHNIQUES; CHILD; CHINCHILLA; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; GENOME, BACTERIAL; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; OTITIS MEDIA; POLYMERASE CHAIN REACTION; SURVIVAL ANALYSIS; TIME FACTORS; VIRULENCE;

EID: 34447331414     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-7-56     Document Type: Article

References (54)

1. Adaptive immunity to nontypeable Haemophilus influenzae. PT King PE Hutchinson PD Johnson PW Holmes NJ Freezer SR Holdsworth, Am J Respir Crit Care Med 2003 15;167 4 587 92 10.1164/rccm.200207-728OC
2. Respiratory infections caused by non-typeable Haemophilus influenzae. TF Murphy, Curr Opin Infect Dis 2003 16 2 129 34 12734445
3. High nasopharyngeal carriage of drug resistant Streptococcus pneumoniae and Haemophilus influenzae in North Indian schoolchildren. A Jain P Kumar S Awasthi, Trop Med Int Health 2005 10 3 234 9 10.1111/j.1365-3156.2004.01379.x 15730507
4. Relative importance of nasopharyngeal versus oropharyngeal sampling for isolation of Streptococcus pneumoniae and Haemophilus influenzae from healthy and sick individuals varies with age. D Greenberg A Broides I Blancovich N Peled N Givon-Lavi R Dagan, J Clin Microbiol 2004 42 10 4604 9 15472316 10.1128/JCM.42.10.4604-4609.2004
5. Characteristics of Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis isolated from the nasopharynges of asymptomatic children and molecular analysis of S. pneumoniae and H. influenzae strain replacement in the nasopharynx. A Sulikowska P Grzesiowski E Sadowy J Fiett W Hryniewicz, J Clin Microbiol 2004 42 9 3942 9 15364973 10.1128/JCM.42.9.3942-3949.2004
6. Protection against development of otitis media induced by NTHi by both active and passive immunization in a chinchilla model of virus-bacterium superinfection. LO Bakaletz BJ Kennedy LA Novotny G Duquesne J Cohen Y Lobet, Infect Immun 1999 67 6 2746 62 10338477
7. The pathogenesis of disease due to nontypeable Haemophilus influenzae. GG Hardy SM Tudor JW St Geme 3rd, Methods Mol Med 2003 71 1 28 12374015
8. Microbiology of acute and chronic sinusitis in children and adults. ER Wald, Am J Med Sci 1998 316 1 13 20 10.1097/00000441-199807000-00003 9671039
9. Animal models for the study of noninvasive Haemophilus influenzae disease: pulmonary clearance systems. EJ Hansen GB Toews, J Infect Dis 1992 165 Suppl 1 S185 7 1588160
10. Identification of the lipooligosaccharide biosynthesis gene lic2B as a putative factor in strains of nontypeable Haemophilus influenzae that cause otitis media. MM Pettigrew B Foxman CF Marrs JR Gilsdorf, Infect Immun 2002 70 7 3551 6 12065495 10.1128/IAI.70.7.3551-3556.2002
11. Differential genome contents of nontypeable Haemophilus influenzae strains from adults with chronic obstructive pulmonary disease. MM Fernaays AJ Lesse S Sethi X Cai TF Murphy, Infect Immun 2006 74 6 3366 74 16714566 10.1128/IAI.01904-05
12. The pathogenicity of Haemophilus influenzae. DC Turk, J Med Microbiol 1984 18 1 16 6146721
13. Role of nontypeable Haemophilus influenzae in pediatric respiratory tract infections. JO Klein, Pediatr Infect Dis J 1997 16 S-8
14. Haemophilus influenzae infections. DM Musher, Hosp Prac (Off Ed) 1983 18 8 158 61 166,169-70.
15. Invasive Haemophilus influenzae in Manitoba, Canada, in the postvaccination era. RS Tsang S Mubareka ML Sill J Wylie S Skinner DK Law, J Clin Microbiol 2006 44 4 1530 5 16597886 10.1128/JCM.44.4.1530-1535.2006
16. Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and upregulates ICAM-1 expression. V Avadhanula CA Rodriguez GC Ulett LO Bakaletz EE Adderson, Infect Immun 2006 74 2 830 8 16428725 10.1128/IAI.74.2.830-838.2006
17. Characterization of genetic and phenotypic diversity of invasive nontypeable Haemophilus influenzae. AL Erwin KL Nelson T Mhlanga-Mutangadura PJ Bonthuis JL Geelhood G Morlin WC Unrath J Campos DW Crook MM Farley FW Henderson RF Jacobs K Muhlemann SW Satola L van Alphen M Golomb AL Smith, Infect Immun 2005 73 9 5853 63 16113304 10.1128/IAI.73.9.5853-5863.2005
18. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. A Harrison DW Dyer A Gillaspy WC Ray R Mungur MB Carson H Zhong J Gipson M Gipson LS Johnson L Lewis LO Bakaletz RS Munson Jr, J Bacteriol 2005 187 13 4627 36 15968074 10.1128/JB.187.13.4627-4636.2005
19. Cloning and sequence analysis of a pilin-like gene from an otitis media isolate of NTHi. LO Bakaletz MA Ahmed PE Kolattukudy DJ Lim LJ Forney, J Infect Dis 1992 165 Suppl 1 S201 3 1588166
20. Survival of nontypeable Haemophilus influenzae in macrophages. JE Craig A Cliffe K Garnett NJ High, FEMS Microbiol Lett 2001 11;203 1 55 61 10.1111/j.1574-6968.2001.tb10820.x
21. Serum resistance in an invasive, nontypeable Haemophilus influenzae strain. BJ Williams G Morlin N Valentine AL Smith, Infect Immun 2001 69 2 695 705 11159957 10.1128/IAI.69.2.695-705.2001
22. Otitis media in children; local immune response to nontypeable Haemophilus influenzae. HL Faden L Brodsky J Bernstein J Stanievich D Krystofik C Shuff JJ Hong PL Ogra, Infect Immun 1989 57 11 3555 9 2807536
23. Release of leukotriene B4 from human neutrophils after interaction with nontypeable Haemophilus influenzae. R Garofalo H Faden S Sharma PL Ogra, Infect Immun 1991 59 11 4221 6 1657784
24. Genetic and phenotypic diversity among ampicillin-resistant, non-beta-lactamase-producing, NTHi isolates. PM Mendelman DO Chaffin JM Musser R De Groot DA Serfass RK Selander, Infect Immun 1987 55 11 2585 9 3499396
25. Identification, distribution and expression of novel genes in 10 clinical isolates of NTHi. K Shen P Antalis J Gladitz S Sayeed A Ahmed S Yu J Hayes S Johnson B Dice R Dopico R Keefe B Janto W Chong J Goodwin RM Wadowsky G Erdos JC Post GD Ehrlich FZ Hu, Infect Immun 2005 73 6 3479 91 15908377 10.1128/IAI.73.6.3479-3491.2005
26. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. RD Fleischmann MD Adams O White RA Clayton EF Kirkness AR Kerlavage CJ Bult J-F Tomb BA Dougherty JM Merrick K McKenney G Sutton W FitzHugh C Fields JD Gocayne J Scott R Shirley L Liu A Glodek JM Kelley JF Weidman CA Phillips T Spriggs E Hedblom MD Cotton TR Utterback MC Hanna DT Nguyen DM Saudek RC Brandon LD Fine JL Fritchman JL Fuhrmann NSM Geoghagen CL Gnehm LA McDonald KV Small CM Fraser HO Smith JC Venter, Science 1995 269 496 512 10.1126/science.7542800 7542800
27. Bacterial Plurality as a General Mechanism Driving Persistence in Chronic Infections. GD Ehrlich FZ Hu K Shen P Stoodley JC Post, Clin Orthop Relat Res 2005 437 20 24 16056021 10.1097/00003086-200508000-00005
28. Intelligent implants to battle biofilms. GD Ehrlich FZ Hu Q Lin JW Costerton JC Post, ASM News 2004 70 3 127 33
29. Diversity and sharing of Haemophilus influenzae strains colonizing healthy children attending day-care centers. RS Farjo B Foxman MJ Patel K Zhang MM Pettigrew SI McCoy CF Marrs JR Gilsdorf, Pediatr Infect Dis J 2004 23 1 41 6 10.1097/01.inf.0000106981.89572.d1 14743045
30. Report of the ASM Task Force of Antibiotic Resistance. GH Cassell GL Archer TR Beam GMJ Goldmann DC Hooper RN Jones SH Kleven J Lederberg SB Levy DH Lein RC Moellering TF O'Brien B Osburn M Osterholm DM Shlaes M Terry SA Tolin A Tomasz, American Society for Microbiology, Washington, D.C. 1994
31. Intracranial complications of acute and chronic infectious ear disease: A problem still with us. D Gower WF McGuirt, Laryngoscope 1983 93 1028 1033 10.1288/00005537-198308000-00010 6877010
32. Neonatal meningitis and mastoiditis caused by Haemophilus influenzae. TB Lee WH Stingle P Ombres JS Lewis LZ Cooper, JAMA 1976 26;235 4 407 9 10.1001/jama.235.4.407
33. NTHi: challenges in developing a vaccine. J Kyd A Cripps, J Biotechnol 1999 20;73 2-3 103 8 10.1016/S0168-1656(99)00113-3
34. Haemophilus influenzae luxS mutants form a biofilm and have increased virulence. DA Daines M Bothwell J Furrer W Unrath K Nelson J Jarish N Melrose L Greiner M Apicella AL Smith, Microb Pathog 2005 39 3 87 96 10.1016/j.micpath. 2005.06.003 16099134
35. Serum and middle ear antibody response in the chinchilla during otitis media with effusion induced by nonviable nontypeable Haemophilus influenzae. TF DeMaria T Yamaguchi LO Bakeletz DJ Lim, J Infect Dis 1992 165 Suppl 1 S196 7 1588163
36. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. GD Ehrlich R Veeh X Wang JW Costerson DJ Hayes FZ Hu BJ Daigle MD Ehrlich JC Post, JAMA 2002 3;287 13 1710 15 10.1001/jama.287.13.1710
37. Development and validation of a multiplex PCR-based assay for the upper respiratory tract bacterial pathogens Haemophilus influenzae, Streptococcus pneumoniae, and Moraxella catarrhalis. JC Post CJ White JJ Aul T Zavoral RM Wadowsky Y Zhang RA Preston GD Ehrlich, Mol Diagn 1996 1 1 29 39 10330195 10.1016/S1084-8592(96)70019-X
38. PCR-based detection of bacterial DNA after microbial treatment is indicative of persistent, viable bacteria in the chinchilla model of otitis media. JC Post JJ Aul GJ White RM Wadowsky T Zavoral R Tabari B Kerber WJ Doyle GD Ehrlich, Am J Otolaryngol 1996 17 2 106 11 10.1016/S0196-0709(96)90005-8 8820185
39. Molecular analysis of bacterial pathogens in otitis media with effusion. JC Post RA Preston JJ Aul M Larkins-Pettigrew J Rydquist-White KW Anderson RM Wadowsky DR Reagan ES Walker LA Kingsley AE Magit GD Ehrlich, JAMA 1995 273 20 1598 604 10.1001/jama.273.20.1598 7745773
40. Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. MG Rayner Y Zhang MC Gorry Y Chen JC Post GD Ehrlich, JAMA 1998 279 296 299 10.1001/jama.279.4.296 9450714
41. Mucin gene cDNA sequence characterization from the chinchilla middle ear epithelium. JE Kerschner T Meyers A Burrows GD Ehrlich JC Post, Intl J Pediatric Otolaryngol 2006 70 8 1449 1456 10.1016/j.ijporl.2006.03.007
42. PCR for capsular typing of Haemophilus influenzae. TJ Falla DW Crook LN Brophy D Maskell JS Kroll ER Moxon, J Clin Microbiol 1994 32 10 2382 6 7814470
43. Identification of Haemophilus influenzae serotypes by standard slide agglutination serotyping and PCR-based capsule typing. LL LaClaira ML Tondella DS Beall CA Noble PL Raghunathan NE Rosenstein T Popovic, J Clin Microbiol 2003 41 393 6 12517878 10.1128/JCM.41.1.393-396.2003
44. R: A Language and Environment for Statistical Computing. R Development Core Team, Vienna, Austria 2006 http://www.R-project.org
45. Primer3 on the WWW for general users and for biologist programmers. S Rozen H Skaletsky, Bioinformatics Methods and Protocols in the series Methods in Molecular Biology Totowa, New Jersey: Humana Press, Krawetz S, Misener S, 2000 365 386
46. AMIgene. SA Hijum AL Zomer OP Kuipers J Kok, Nucleic Acids Res 2003 31 22 e144 14602937 10.1093/nar/gng144
47. Improved tools for biological sequence comparison. WR Pearson DJ Lipman, Proc Natl Acad Sci USA 1988 85 8 2444 8 3162770 10.1073/pnas.85.8.2444
48. AK Jain RC Dubes, Algorithms for Clustering Data Englewood Cliffs, New Jersey: Prentice Hall 1988
49. Blocking of fimbria-mediated adherence of Haemophilus influenzae by sialyl gangliosides. L van Alphen L Geelen-van den Broek L Blaas M van Ham J Dankert, Infect Immun 1991 59 4473 4477 1682262
50. Prevalence of the hifBC, hmw1A, hmw2A, hmwC, and hia genes in Haemophilus influenzae isolates. IZ Ecevit KW McCrea MM Pettigrew A Sean CF Marrs JR Gilsdorf, J Clin Microbiol 2004 42 3065 3072 15243061 10.1128/JCM.42.7.3065- 3072.2004
51. Phosphorylcholine decreases early inflammation and promotes establishment of stable biofilm communities of nontypeable Haemophilus influenzae strain 86-028 NP in a chinchilla model of otitis media. W Hong K Mason J Juriscek L Novotny LO Bakaletz WE Swords, Infect Immun 2007 75 2 958 65 17130253 10.1128/IAI.01691-06
52. Role of the two-component signal transduction and the phosphoenolpyruvate:carbohydrate phosphotransferase systems in competence development of Haemophilus influenzae Rd. ML Gwinn D Yi HO Smith JF Tomb, J Bacteriol 1996 178 21 6366 8 8892843
53. Frequency and distribution of DNA uptake signal sequences in the Haemophilus influenzae Rd genome. HO Smith JF Tomb BA Dougherty RD Fleischmann JC Venter, Science 1995 28;269 5223 538 40 10.1126/science.7542802
54. Differences in genetic diversity of nonencapsulated Haemophilus influenzae from various diseases. L van Alphen DA Caugant B Duim M O'Rourke L Bowler, Microbiol 1997 143 Part 4 1423 31