Adhesin genes and serum resistance in Haemophilus influenzae type f isolates

Journal of Medical Microbiology

Volumn 62, Issue PART4, 2013, Pages 514-524

  Watson, Michael E ^a   Nelson, Kevin L ^b   Nguyen, Victoria ^b   Burnham, Carey Ann D ^a   Clarridge, Jill E ^c   Qin, Xuan ^c   Smith, Arnold L ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; LIPOOLIGOSACCHARIDE;

ARTICLE; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; CONTROLLED STUDY; DNA FINGERPRINTING; GENE LOCUS; HAEMOPHILUS INFLUENZAE; NONHUMAN; OPERON; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

EID: 84875200559     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.052175-0     Document Type: Article

References (62)

1. Adam, H. J., Richardson, S. E., Jamieson, F. B., Rawte, P., Low, D. E. & Fisman, D. N. (2010). Changing epidemiology of invasive Haemophilus influenzae in Ontario, Canada: evidence for herd effects and strain replacement due to Hib vaccination. Vaccine 28, 4073-4078.
2. Agrawal, A. & Murphy, T. F. (2011). Haemophilus influenzae infections in the H. influenzae type b conjugate vaccine era. J Clin Microbiol 49, 3728-3732.
3. Aubrey, R. & Tang, C. (2003). The pathogenesis of disease due to type b Haemophilus influenzae. Methods Mol Med 71, 29-50.
4. Barenkamp, S. J. & Leininger, E. (1992). Cloning, expression, and DNA sequence analysis of genes encoding nontypeable Haemophilus influenzae high-molecular-weight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis. Infect Immun 60, 1302-1313.
5. Barenkamp, S. J. & St Geme, J. W., III (1996). Identification of a second family of high-molecular-weight adhesion proteins expressed by non-typable Haemophilus influenzae. Mol Microbiol 19, 1215-1223.
6. Berndsen, M. R., Erlendsdottir, H. & Gottfredsson, M. (2011). Evolving epidemiology of invasive Haemophilus infections in the post-vaccination era: results from a long-term population-based study. Clin Microbiol Infect 18, 918-923.
7. Bruun, B., Gahrn-Hansen, B., Westh, H. & Kilian, M. (2004). Clonal relationship of recent invasive Haemophilus influenzae serotype f isolates from Denmark and the United States. J Med Microbiol 53, 1161-1165.
8. Campos, J., Román, F., Pé rez-Vázquez, M., Aracil, B., Oteo, J., Cercenado, E. & the Spanish Study Group for H. influenzae type f (2003). Antibiotic resistance and clinical significance of Haemophilus influenzae type f. J Antimicrob Chemother 52, 961-966.
9. Dabernat, H. & Delmas, C. (2012). Epidemiology and evolution of antibiotic resistance of Haemophilus influenzae in children 5 years of age or less in France, 2001-2008: a retrospective database analysis. Eur J Clin Microbiol Infect Dis 31, 2745-2753.
10. Erwin, A. L., Nelson, K. L., Mhlanga-Mutangadura, T., Bonthuis, P. J., Geelhood, J. L., Morlin, G., Unrath, W. C., Campos, J., Crook, D. W. & other authors (2005). Characterization of genetic and phenotypic diversity of invasive nontypeable Haemophilus influenzae. Infect Immun 73, 5853-5863.
11. Erwin, A. L., Allen, S., Ho, D. K., Bonthuis, P. J., Jarisch, J., Nelson, K. L., Tsao, D. L., Unrath, W. C., Watson, M. E., Jr & other authors (2006a). Role of lgtC in resistance of nontypeable Haemophilus influenzae strain R2866 to human serum. Infect Immun 74, 6226-6235.
12. Erwin, A. L., Bonthuis, P. J., Geelhood, J. L., Nelson, K. L., McCrea, K. W., Gilsdorf, J. R. & Smith, A. L. (2006b). Heterogeneity in tandem octanucleotides within Haemophilus influenzae lipopolysaccharide biosynthetic gene losA affects serum resistance. Infect Immun 74, 3408-3414.
13. Falla, T. J., Crook, D. W., Brophy, L. N., Maskell, D., Kroll, J. S. & Moxon, E. R. (1994). PCR for capsular typing of Haemophilus influenzae. J Clin Microbiol 32, 2382-2386.
14. Falla, T. J., Crook, D. W., Anderson, E. C., Ward, J. I., Santosham, M., Eskola, J. & Moxon, E. R. (1995). Characterization of capsular genes in Haemophilus influenzae isolates from H. influenzae type b vaccine recipients. J Infect Dis 171, 1075-1076.
15. Fickweiler, K., Borte, M., Fasshauer, M., Spencker, F. B., Handrick, W. & Rodloff, A. C. (2004). Meningitis due to Haemophilus influenzae type f in an 8-year-old girl with congenital humoral immunodeficiency. Infection 32, 112-115.
16. Harrison, A., Dyer, D. W., Gillaspy, A., Ray, W. C., Mungur, R., Carson, M. B., Zhong, H., Gipson, J., Gipson, M. & other authors (2005). Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J Bacteriol 187, 4627-4636.
17. Hasegawa, K., Kobayashi, R., Takada, E., Ono, A., Chiba, N., Morozumi, M., Iwata, S., Sunakawa, K. & Ubukata, K. on behalf of the Working Group of the Nationwide Surveillance for Bacterial Meningitis (2006). High prevalence of type b b-lactamase-nonproducing ampicillin-resistant Haemophilus influenzae in meningitis: the situation in Japan where Hib vaccine has not been introduced. J Antimicrob Chemother 57, 1077-1082.
18. Healy, M., Huong, J., Bittner, T., Lising, M., Frye, S., Raza, S., Schrock, R., Manry, J., Renwick, A. & other authors (2005a). Microbial DNA typing by automated repetitive-sequence-based PCR. J Clin Microbiol 43, 199-207.
19. Healy, M., Reece, K., Walton, D., Huong, J., Frye, S., Raad, I. I. & Kontoyiannis, D. P. (2005b). Use of the Diversi Lab System for species and strain differentiation of Fusarium species isolates. J Clin Microbiol 43, 5278-5280.
20. High, N. J., Jennings, M. P. & Moxon, E. R. (1996). Tandem repeats of the tetramer 59-CAAT-39 present in lic2A are required for phase variation but not lipopolysaccharide biosynthesis in Haemophilus influenzae. Mol Microbiol 20, 165-174.
21. Hood, D. W., Deadman, M. E., Cox, A. D., Makepeace, K., Martin, A., Richards, J. C. & Moxon, E. R. (2004). Three genes, lgtF, lic2C and lpsA, have a primary role in determining the pattern of oligosaccharide extension from the inner core of Haemophilus influenzae LPS. Microbiology 150, 2089-2097.
22. Hulton, C. S., Higgins, C. F. & Sharp, P. M. (1991). ERIC sequences: a novel family of repetitive elements in the genomes of Escherichia coli, Salmonella typhimurium and other enterobacteria. Mol Microbiol 5, 825-834.
23. Kang, H. P. & Dunne, W. M. (2003). Stability of repetitive-sequence PCR patterns with respect to culture age and subculture frequency. J Clin Microbiol 41, 2694-2696.
24. Kilian, M. (1976). A taxonomic study of the genus Haemophilus, with the proposal of a new species. J Gen Microbiol 93, 9-62.
25. Ladhani, S. N. (2012). Two decades of experience with the Haemophilus influenzae serotype b conjugate vaccine in the United Kingdom. Clin Ther 34, 385-399.
26. Ladhani, S., Slack, M. P., Heath, P. T., Von Gottberg, A., Chandra, M., Ramsay, M. E. & European Union Invasive Bacterial Infection Surveillance participants (2010). Invasive Haemophilus influenzae disease, Europe, 1996-2006. Emerg Infect Dis 16, 455-463.
27. Ladhani, S. N., Collins, S., Vickers, A., Litt, D. J., Crawford, C., Ramsay, M. E. & Slack, M. P. (2012). Invasive Haemophilus influenzae serotype e and f disease, England and Wales. Emerg Infect Dis 18, 725-732.
28. MacNeil, J. R., Cohn, A. C., Farley, M., Mair, R., Baumbach, J., Bennett, N., Gershman, K., Harrison, L. H., Lynfield, R. & other authors (2011). Current epidemiology and trends in invasive Haemophilus influenzae disease-United States, 1989-2008. Clin Infect Dis 53, 1230-1236.
29. Meats, E., Feil, E. J., Stringer, S., Cody, A. J., Goldstein, R., Kroll, J. S., Popovic, T. & Spratt, B. G. (2003). Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J Clin Microbiol 41, 1623-1636.
30. Mhlanga-Mutangadura, T., Morlin, G., Smith, A. L., Eisenstark, A. & Golomb, M. (1998). Evolution of the major pilus gene cluster of Haemophilus influenzae. J Bacteriol 180, 4693-4703.
31. Morris, S. K., Moss, W. J. & Halsey, N. (2008). Haemophilus influenzae type b conjugate vaccine use and effectiveness. Lancet Infect Dis 8, 435-443.
32. Moxon, E. R. & Kroll, J. S. (1988). Type b capsular polysaccharide as a virulence factor of Haemophilus influenzae. Vaccine 6, 113-115.
33. Murray, P. R., Baron, E. J., Jorgensen, J. H., Pfaller, M. A. & Yolken, R. H. (eds) (2003). Manual of Clinical Microbiology. Washington, DC: American Society for Microbiology.
34. Nakamura, S., Shchepetov, M., Dalia, A. B., Clark, S. E., Murphy, T. F., Sethi, S., Gilsdorf, J. R., Smith, A. L. & Weiser, J. N. (2011). Molecular basis of increased serum resistance among pulmonary isolates of non-typeable Haemophilus influenzae. PLoS Pathog 7, e1001247.
35. Nelson, K. L. & Smith, A. L. (2010). Determination of capsulation status in Haemophilus influenzae by multiplex polymerase chain reaction. Diagn Microbiol Infect Dis 66, 235-240.
36. Nitta, D. M., Jackson, M. A., Burry, V. F. & Olson, L. C. (1995). Invasive Haemophilus influenzae type f disease. Pediatr Infect Dis J 14, 157-160.
37. Nizet, V., Colina, K. F., Almquist, J. R., Rubens, C. E. & Smith, A. L. (1996). A virulent nonencapsulated Haemophilus influenzae. J Infect Dis 173, 180-186.
38. Omikunle, A., Takahashi, S., Ogilvie, C. L., Wang, Y., Rodriguez, C. A., St Geme, J. W., III & Adderson, E. E. (2002). Limited genetic diversity of recent invasive isolates of non-serotype b encapsulated Haemophilus influenzae. J Clin Microbiol 40, 1264-1270.
39. Philpott-Howard, J. & Williams, J. D. (1982). Increase in antibiotic resistance in Haemophilus influenzae in the United Kingdom since 1977: report of study group. Br Med J (Clin Res Ed) 284, 1597-1599.
40. Pichichero, M. E., Loeb, M., Anderson & Smith, D. H. (1982). Do pili play a role in pathogenicity of Haemophilus influenzae type b? Lancet 320, 960-962.
41. Pittman, M. (1931). Variation and type specificity in the bacterial species Hemophilus influenzae. J Exp Med 53, 471-492.
42. Resman, F., Ristovski, M., Ahl, J., Forsgren, A., Gilsdorf, J. R., Jasir, A., Kaijser, B., Kronvall, G. & Riesbeck, K. (2011a). Invasive disease caused by Haemophilus influenzae in Sweden 1997-2009; evidence of increasing incidence and clinical burden of non-type b strains. Clin Microbiol Infect 17, 1638-1645.
43. Resman, F., Svensjö, T., Ünal, C., Cronqvist, J., Brorson, H., Odenholt, I. & Riesbeck, K. (2011b). Necrotizing myositis and septic shock caused by Haemophilus influenzae type f in a previously healthy man diagnosed with an IgG3 and a mannose-binding lectin deficiency. Scand J Infect Dis 43, 972-976.
44. Rodriguez, C. A., Avadhanula, V., Buscher, A., Smith, A. L., St Geme, J. W., III & Adderson, E. E. (2003). Prevalence and distribution of adhesins in invasive non-type b encapsulated Haemophilus influenzae. Infect Immun 71, 1635-1642.
45. Rubach, M. P., Bender, J. M., Mottice, S., Hanson, K., Weng, H. Y., Korgenski, K., Daly, J. A. & Pavia, A. T. (2011). Increasing incidence of invasive Haemophilus influenzae disease in adults, Utah, USA. Emerg Infect Dis 17, 1645-1650.
46. Scheifele, D. W., Syriopoulou, V. P., Harding, A. L., Emerson, B. B. & Smith, A. L. (1976). Evaluation of a rapid b-lactamase test for detecting ampicillin-resistant strains of Hemophilus influenzae type b. Pediatrics 58, 382-387.
47. St Geme, J. W., III, Falkow, S. & Barenkamp, S. J. (1993). Highmolecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc Natl Acad Sci U S A 90, 2875-2879.
48. St Geme, J. W., III, Cutter, D. & Barenkamp, S. J. (1996). Characterization of the genetic locus encoding Haemophilus influenzae type b surface fibrils. J Bacteriol 178, 6281-6287.
49. St Geme, J. W., III, Kumar, V. V., Cutter, D. & Barenkamp, S. J. (1998). Prevalence and distribution of the hmw and hia genes and the HMW and Hia adhesins among genetically diverse strains of nontypeable Haemophilus influenzae. Infect Immun 66, 364-368.
50. Takala, A. K., Eskola, J., Leinonen, M., Käyhty, H., Nissinen, A., Pekkanen, E. & Mäkelä, P. H. (1991). Reduction of oropharyngeal carriage of Haemophilus influenzae type b (Hib) in children immunized with an Hib conjugate vaccine. J Infect Dis 164, 982-986.
51. Tsang, R. (2007). Capsule switching and capsule replacement in vaccine-preventable bacterial diseases. Lancet Infect Dis 7, 569-570.
52. Tsang, R. S., Mubareka, S., Sill, M. L., Wylie, J., Skinner, S. & Law, D. K. (2006). Invasive Haemophilus influenzae in Manitoba, Canada, in the postvaccination era. J Clin Microbiol 44, 1530-1535.
53. Ubukata, K., Shibasaki, Y., Yamamoto, K., Chiba, N., Hasegawa, K., Takeuchi, Y., Sunakawa, K., Inoue, M. & Konno, M. (2001). Association of amino acid substitutions in penicillin-binding protein 3 with b-lactam resistance in b-lactamase-negative ampicillinresistant Haemophilus influenzae. Antimicrob Agents Chemother 45, 1693-1699.
54. Urwin, G., Krohn, J. A., Deaver-Robinson, K., Wenger, J. D., Farley, M. M. & the Haemophilus influenzae Study Group (1996). Invasive disease due to Haemophilus influenzae serotype f: clinical and epidemiologic characteristics in the H. influenzae serotype b vaccine era. Clin Infect Dis 22, 1069-1076.
55. Ward, J. I. (1996). Invasive infections due to Haemophilus influenzae serotype f (Hif)-is Hif an emerging pathogen? Clin Infect Dis 22, 1077-1078.
56. Watson, M. E., Jr, Burns, J. L. & Smith, A. L. (2004). Hypermutable Haemophilus influenzae with mutations in mutS are found in cystic fibrosis sputum. Microbiology 150, 2947-2958.
57. Watson, M. E., Jr, Davila, S. Z., Burnham, C. A., Nguyen, V., Nelson, K. L., Smith, A. L. & Storch, G. A. (2011). Thigh abscess due to Haemophilus influenzae type f in a human immunodeficiency viruspositive child. Infect Dis Clin Pract 19, e21-e23.
58. Weiser, J. N. & Pan, N. (1998). Adaptation of Haemophilus influenzae to acquired and innate humoral immunity based on phase variation of lipopolysaccharide. Mol Microbiol 30, 767-775.
59. Weller, P. F., Smith, A. L., Anderson, P. & Smith, D. H. (1977). The role of encapsulation and host age in the clearance of Haemophilus influenzae bacteremia. J Infect Dis 135, 34-41.
60. Wilcox, K. W. & Smith, H. O. (1975). Isolation and characterization of mutants of Haemophilus influenzae deficient in an adenosine 59-triphosphate-dependent deoxyribonuclease activity. J Bacteriol 122, 443-453.
61. Williams, B. J., Morlin, G., Valentine, N. & Smith, A. L. (2001). Serum resistance in an invasive, nontypeable Haemophilus influenzae strain. Infect Immun 69, 695-705.
62. Zwahlen, A., Winkelstein, J. A. & Moxon, E. R. (1983). Surface determinants of Haemophilus influenzae pathogenicity: comparative virulence of capsular transformants in normal and complementdepleted rats. J Infect Dis 148, 385-394.