Molecular tools for differentiation of non-typeable Haemophilus influenzae from Haemophilus haemolyticus

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages 664-

  Pickering, Janessa ^a   Richmond, Peter C ^a,b   Kirkham, Lea Ann S ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Culture; Haemophilus haemolyticus; identification; Molecular differentiation; NTHi

Indexed keywords

DNA 16S; EPITOPE; HEMOLYSIN; LIPOOLIGOSACCHARIDE;

BACTERIAL GENE; BACTERIUM IDENTIFICATION; DNA POLYMORPHISM; DOT HYBRIDIZATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC HETEROGENEITY; GENOME ANALYSIS; HAEMOPHILUS HAEMOLYTICUS; HAEMOPHILUS INFECTION; HAEMOPHILUS INFLUENZAE; LABORATORY DIAGNOSIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DIAGNOSIS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NONTYPEABLE HAEMOPHILUS INFLUENZAE; PHYLOGENETIC TREE; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY TRACT INFECTION; SHORT SURVEY; SPECIES IDENTIFICATION;

HAEMOPHILUS HAEMOLYTICUS; HAEMOPHILUS INFLUENZAE;

EID: 84920691828     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00664     Document Type: Short Survey

References (43)

1. Abdeldaim, G. M., Stralin, K., Kirsebom, L. A., Olcen, P., Blomberg, J., and Herrmann, B. (2009). Detection of Haemophilus influenzae in respiratory secretions from pneumonia patients by quantitative real-time polymerase chain reaction. Diagn. Microbiol. Infect. Dis. 64, 366-373. doi: 10.1016/j.diagmicrobio.2009.03.030
2. Abdeldaim, G. M., Stralin, K., Olcen, P., Blomberg, J., Molling, P., and Herrmann, B. (2013). Quantitative fucK gene polymerase chain reaction on sputum and nasopharyngeal secretions to detect Haemophilus influenzae pneumonia. Diagn. Microbiol. Infect. Dis. 76, 141-146. doi: 10.1016/j.diagmicrobio.2013.02.015
3. Anderson, R., Wang, X., Briere, E. C., Katz, L. S., Cohn, A. C., Clark, T. A., et al. (2012). Haemophilus haemolyticus isolates causing clinical disease. J. Clin. Microbiol. 50, 2462-2465. doi: 10.1128/JCM.06575-11
4. Binks, M. J., Temple, B., Kirkham, L. A., Wiertsema, S. P., Dunne, E. M., Richmond, P. C., et al. (2012). Molecular surveillance of true nontypeable Haemophilus influenzae: an evaluation of PCR screening assays. PLoS ONE 7:e34083. doi: 10.1371/journal.pone.0034083
5. Broom, A., and Sneath, P. H. (1981). Numerical taxonomy of Haemophilus. J. Gen. Microbiol. 126, 123-149.
6. Chang, A., Adlowitz, D. G., Yellamatty, E., and Pichichero, M. (2010). Haemophilus influenzae outer membrane protein P6 molecular characterization may not differentiate all strains of H. Influenzae from H. haemolyticus. J. Clin. Microbiol. 48, 3756-3757. doi: 10.1128/JCM.01255-10
7. Corless, C. E., Guiver, M., Borrow, R., Edwards-Jones, V., Fox, A. J., and Kaczmarski, E. B. (2001). Simultaneous detection of Neisseria meningitidis, Haemophilus influenzae, and Streptococcus pneumoniae in suspected cases of meningitis and septicemia using real-time PCR. J. Clin. Microbiol. 39, 1553-1558. doi: 10.1128/JCM.39.4.1553-1558.2001
8. De Chiara, M., Hood, D., Muzzi, A., Pickard, D. J., Perkins, T., Pizza, M., et al. (2014). Genome sequencing of disease and carriage isolates of nontypeable Haemophilus influenzae identifies discrete population structure. Proc. Natl. Acad. Sci. U.S.A. 111, 5439-5444. doi: 10.1073/pnas.1403353111
9. De Santo, D. A., and White, M. (1933). Hemophilus hemolyticus endocarditis. Am. J. Pathol. 9, 381-392.
10. Frickmann, H., Christner, M., Donat, M., Berger, A., Essig, A., Podbielski, A., et al. (2013). Rapid discrimination of Haemophilus influenzae, H. parainfluenzae, and H. haemolyticus by fluorescence in situ hybridization (FISH) and two matrix-assisted laser-desorption-ionization time-of-flight mass spectrometry (MALDI-TOF-MS) platforms. PLoS ONE 8:e63222. doi: 10.1371/journal.pone.0063222
11. Fung, W. W., O'dwyer, C. A., Sinha, S., Brauer, A. L., Murphy, T. F., Kroll, J. S., et al. (2006). Presence of copper- and zinc-containing superoxide dismutase in commensal Haemophilus haemolyticus isolates can be used as a marker to discriminate them from nontypeable H. influenzae isolates. J. Clin. Microbiol. 44, 4222-4226. doi: 10.1128/JCM.01376-06
12. Hare, K. M., Binks, M. J., Grimwood, K., Chang, A. B., Leach, A. J., and Smith-Vaughan, H. (2012). Culture and PCR detection of Haemophilus influenzae and Haemophilus haemolyticus in Australian Indigenous children with bronchiectasis. J. Clin. Microbiol. 50, 2444-2445. doi: 10.1128/JCM.00566-12
13. Johnson, R. W., McGillivary, G., Denoel, P., Poolman, J., and Bakaletz, L. O. (2011). Abrogation of nontypeable Haemophilus influenzae protein D function reduces phosphorylcholine decoration, adherence to airway epithelial cells, and fitness in a chinchilla model of otitis media. Vaccine 29, 1211-1221. doi: 10.1016/j.vaccine.2010.12.003
14. Kaur, R., Chang, A., Xu, Q., Casey, J. R., and Pichichero, M. E. (2011). Phylogenetic relatedness and diversity of non-typable Haemophilus influenzae in the nasopharynx and middle ear fluid of children with acute otitis media. J. Med. Microbiol. 60, 1841-1848. doi: 10.1099/jmm.0.034041-0
15. Kilian, M. (1976a). The haemolytic activity of Haemophilus species. Acta Pathol. Microbiol. Scand. B 84B, 339-341.
16. Kilian, M. (1976b). A taxonomic study of the genus Haemophilus, with the proposal of a new species. J. Gen. Microbiol. 93, 9-62. doi: 10.1099/00221287-93-1-9
17. Kirkham, L. A., Wiertsema, S. P., Mowe, E. N., Bowman, J. M., Riley, T. V., and Richmond, P. C. (2010). Nasopharyngeal carriage of Haemophilus haemolyticus in otitis-prone and healthy children. J. Clin. Microbiol. 48, 2557-2559. doi: 10.1128/JCM.00069-10
18. McCrea, K. W., Wang, M. L., Xie, J., Sandstedt, S. A., Davis, G. S., Lee, J. H., et al. (2010a). Prevalence of the sodC gene in nontypeable Haemophilus influenzae and Haemophilus haemolyticus by microarray-based hybridization. J. Clin. Microbiol. 48, 714-719. doi: 10.1128/JCM.01416-09
19. McCrea, K. W., Xie, J., Lacross, N., Patel, M., Mukundan, D., Murphy, T. F., et al. (2008). Relationships of nontypeable Haemophilus influenzae strains to hemolytic and nonhemolytic Haemophilus haemolyticus strains. J. Clin. Microbiol. 46, 406-416. doi: 10.1128/JCM.01832-07
20. McCrea, K. W., Xie, J., Marrs, C. F., and Gilsdorf, J. R. (2010b). Prevalence of genetic differences in phosphorylcholine expression between nontypeable Haemophilus influenzae and Haemophilus haemolyticus. BMC Microbiol. 10:286. doi: 10.1186/1471-2180-10-286
21. Miller, C., and Branch, A. (1923). Subacute bacterial endocarditis due to a hemolytic hemophilic bacillus. Arch. Intern. Med. 32, 911-923. doi: 10.1001/archinte.1923.00110240104006
22. Morton, D. J., Hempel, R. J., Whitby, P. W., Seale, T. W., and Stull, T. L. (2012). An invasive Haemophilus haemolyticus isolate. J. Clin. Microbiol. 50, 1502-1503. doi: 10.1128/JCM.06688-11
23. Murphy, T. F., Brauer, A. L., Sethi, S., Kilian, M., Cai, X., and Lesse, A. J. (2007). Haemophilus haemolyticus: a human respiratory tract commensal to be distinguished from Haemophilus influenzae. J. Infect. Dis. 195, 81-89. doi: 10.1086/509824
24. Nelson, M. B., Munson, R. S. Jr., Apicella, M. A., Sikkema, D. J., Molleston, J. P., and Murphy, T. F. (1991). Molecular conservation of the P6 outer membrane protein among strains of Haemophilus influenzae: analysis of antigenic determinants, gene sequences, and restriction fragment length polymorphisms. Infect. Immun. 59, 2658-2663.
25. Norskov-Lauritsen, N. (2009). Detection of cryptic genospecies misidentified as Haemophilus influenzae in routine clinical samples by assessment of marker genes fucK, hap, and sodC. J. Clin. Microbiol. 47, 2590-2592. doi: 10.1128/JCM.00013-09
26. Norskov-Lauritsen, N. (2011). Increased level of intragenomic 16S rRNA gene heterogeneity in commensal strains closely related to Haemophilus influenzae. Microbiology 157, 1050-1055. doi: 10.1099/mic.0.047233-0
27. Norskov-Lauritsen, N. (2014). Classification, identification, and clinical significance of haemophilus and aggregatibacter species with host specificity for humans. Clin. Microbiol. Rev. 27, 214-240. doi: 10.1128/CMR.00103-13
28. Norskov-Lauritsen, N., Bruun, B., and Kilian, M. (2005). Multilocus sequence phylogenetic study of the genus Haemophilus with description of Haemophilus pittmaniae sp. nov. Int. J. Syst. Evol. Microbiol. 55, 449-456. doi: 10.1099/ijs.0.63325-0
29. Norskov-Lauritsen, N., Overballe, M. D., and Kilian, M. (2009). Delineation of the species Haemophilus influenzae by phenotype, multilocus sequence phylogeny, and detection of marker genes. J. Bacteriol. 191, 822-831. doi: 10.1128/JB.00782-08
30. Pickering, J., Binks, M. J., Beissbarth, J., Hare, K. M., Kirkham, L. A., and Smith-Vaughan, H. (2014a). A PCR-high-resolution melt assay for rapid differentiation of nontypeable Haemophilus influenzae and Haemophilus haemolyticus. J. Clin. Microbiol. 52, 663-667. doi: 10.1128/JCM.02191-13
31. Pickering, J., Smith-Vaughan, H., Beissbarth, J., Bowman, J. M., Wiertsema, S., Riley, T. V., et al. (2014b). Diversity of nontypeable Haemophilus influenzae strains colonizing Australian Aboriginal and non-Aboriginal children. J. Clin. Microbiol. 52, 1352-1357. doi: 10.1128/JCM.03448-13
32. Puig, C., Calatayud, L., Marti, S., Tubau, F., Garcia-Vidal, C., Carratala, J., et al. (2013). Molecular epidemiology of nontypeable Haemophilus influenzae causing community-acquired pneumonia in adults. PLoS ONE 8:e82515. doi: 10.1371/journal.pone.0082515
33. Ridderberg, W., Fenger, M. G., and Norskov-Lauritsen, N. (2010). Haemophilus influenzae may be untypable by the multilocus sequence typing scheme due to a complete deletion of the fucose operon. J. Med. Microbiol. 59, 740-742. doi: 10.1099/jmm.0.018424-0
34. Sandstedt, S. A., Zhang, L., Patel, M., McCrea, K. W., Qin, Z., Marrs, C. F., et al. (2008). Comparison of laboratory-based and phylogenetic methods to distinguish between Haemophilus influenzae and H. haemolyticus. J. Microbiol. Methods 75, 369-371. doi: 10.1016/j.mimet.2008.06.023
35. Schumacher, S. K., Marchant, C. D., Loughlin, A. M., Bouchet, V., Stevenson, A., and Pelton, S. I. (2012). Prevalence and genetic diversity of nontypeable Haemophilus influenzae in the respiratory tract of infants and primary caregivers. Pediatr. Infect. Dis. J. 31, 145-149. doi: 10.1097/INF.0b013e31823aaeb3
36. Smith-Vaughan, H. C., Chang, A. B., Sarovich, D. S., Marsh, R. L., Grimwood, K., Leach, A. J., et al. (2014). Absence of an important vaccine and diagnostic target in carriage- and disease-related nontypeable Haemophilus influenzae. Clin. Vaccine Immunol. 21, 250-252. doi: 10.1128/CVI.00632-13
37. Sondergaard, A., Witherden, E. A., Norskov-Lauritsen, L., and Tristram, S. (2014). "Horizontal transfer of chromosomally-encoded resistance to beta-lactam antibiotics between Haemophilus influenzae and Haemophilus haemolyticus," in International Pasteurellaceae Conference 2014 (Prato).
38. Song, X. M., Forsgren, A., and Janson, H. (1995). The gene encoding protein D (hpd) is highly conserved among Haemophilus influenzae type b and nontypeable strains. Infect. Immun. 63, 696-699.
39. Tateno, Y., Takezaki, N., and Nei, M. (1994). Relative efficiencies of the maximum-likelihood, neighbor-joining, and maximum-parsimony methods when substitution rate varies with site. Mol. Biol. Evol. 11, 261-277.
40. Theodore, M. J., Anderson, R. D., Wang, X., Katz, L. S., Vuong, J. T., Bell, M. E., et al. (2012). Evaluation of new biomarker genes for differentiating Haemophilus influenzae from Haemophilus haemolyticus. J. Clin. Microbiol. 50, 1422-1424. doi: 10.1128/JCM.06702-11
41. Wang, X., Mair, R., Hatcher, C., Theodore, M. J., Edmond, K., Wu, H. M., et al. (2011). Detection of bacterial pathogens in Mongolia meningitis surveillance with a new real-time PCR assay to detect Haemophilus influenzae. Int. J. Med. Microbiol. 301, 303-309. doi: 10.1016/j.ijmm.2010.11.004
42. Witherden, E. A., Kunde, D., and Tristram, S. G. (2013). PCR screening for the N526K substitution in isolates of Haemophilus influenzae and Haemophilus haemolyticus. J. Antimicrob. Chemother. 68, 2255-2258. doi: 10.1093/jac/dkt189
43. Zhu, B., Xiao, D., Zhang, H., Zhang, Y., Gao, Y., Xu, L., et al. (2013). MALDI-TOF MS distinctly differentiates nontypable Haemophilus influenzae from Haemophilus haemolyticus. PLoS ONE 8:e56139. doi: 10.1371/journal.pone.0056139