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  • 1 Fachbereich Tropenmedizin am Bernhard-Nocht Institut, Bundeswehrkrankenhaus Hamburg, Hamburg, Germany
  • | 2 Institut für Mikrobiologie, Virologie und Hygiene, Universitätsmedizin Rostock, Rostock, Germany
  • | 3 Institut für Mikrobiologie, Virologie und Hygiene, Universitätsmedizin Ulm, Ulm, Germany
  • | 4 AG Infektionsepidemiologie, Bernhard-Nocht Institut für Tropenmedizin Hamburg, Hamburg, Germany
  • | 5 UMG-Labor — Institut für Klinische Chemie/Zentrallabor, Universitätsmedizin Göttingen, Göttingen, Germany
  • | 6 Institut für Medizinische Mikrobiologie, Universitätsmedizin Göttingen, Kreuzbergring 57, D-37075, Göttingen, Germany
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Abstract

Diagnostic misidentifications of commensalic Haemophilus haemolyticus as pathogenic Haemophilus influenzae are frequent. This pilot study evaluates whether isolations of H. haemolyticus are frequent enough in Germany to cause a relevant diagnostic problem, considering the fact that even H. influenzae is a mere colonizer in about 30% of isolations.

In microbiological laboratories of two hospitals located in Northern and Southern Germany, the distribution of Haemophilus spp. was analyzed during a six-month-period. Site of infection, sex, and age of the patients was taken into consideration.

A total of 77 Haemophilus spp. isolates was acquired and discriminated on species level, comprising: 48 H. influenzae, 25 Haemophilus parainfluenzae, 3 H. haemolyticus, and 1 Haemophilus parahaemolyticus. The proportion of H. haemolyticus was calculated to range between 1.2% and 16.2 % within the 95% confidence limits. Commensalic Haemophilus spp. were isolated from oropharynx-associated sites only. H. influenzae, in contrast, was detected in clinically relevant materials like lower respiratory materials and conjunctiva swabs.

Altogether, there was a low proportion of clinical H. haemolyticus isolates. Accordingly, the problem of unnecessary antibiotic therapies due to misidentifications of H. haemolyticus as H. influenzae is quantitatively negligible compared with the risk of confusing H. influenzae colonizations with infections.

  • 1. WJ Mogabgab 1963 Viruses associated with upper respiratory illnesses in adults Ann Intern Med 59 306 322.

  • 2. AZ Kapikian KM Johnson RM Chanock JA Bell LM Dyke RE Iler 1964 A pilot study of acute respiratory illnesses on a college campus Am Rev Respir Dis 90 175 182.

    • Search Google Scholar
    • Export Citation
  • 3. PM Poole JO Tobin 1973 Viral and epidemiological findings in MRC/PHLS surveys of respiratory disease in hospital and general practice Postgrad Med J 49 778 787.

    • Search Google Scholar
    • Export Citation
  • 4. KG Nicholson J Kent V Hammersley E Cancio 1997 Acute viral infections of upper respiratory tract in elderly people living in the community: comparative, prospective, population based study of disease burden BMJ 315 10 0.

    • Search Google Scholar
    • Export Citation
  • 5. R Gonzales JG Bartlett RE Besser JM Hickner MA Hoffman ai]JR, Sande 2001 Principles of appropriate antibiotic use for treatment of nonspecific upper respiratory tract infections in adults: background Ann Intern Med 134 490 494.

    • Search Google Scholar
    • Export Citation
  • 6. R Jain R Lodha SH Kabra 2001 Upper respiratory tract infections Indian J Pediatr 68 1135 1138.

  • 7. MMH Kusel NH de Klerk PG Holt T Kebadze SL Johnston PD Sly 2006 Role of respiratory viruses in acute upper and lower respiratory tract illness in the first year of life Pediatr Infect Dis J 25 680 686.

    • Search Google Scholar
    • Export Citation
  • 8. DC Turk 1984 The pathogenicity of Haemophilus influenzae J Med Microbiol 18 1 16.

  • 9. I Brook 2009 Current management of upper respiratory tract and head and neck infections Eur Arch Otorhinolaryngol 266 315 323.

  • 10. AE Zautner M Krause G Stropahl S Holtfreter H Frickmann C Maletzki B Kreikemeyer HW Pau A Podbielski 2010 Intracellular persisting Staphylococcus aureus is the major pathogen in recurrent tonsillitis PLoS One 5 e9452.

    • Search Google Scholar
    • Export Citation
  • 11. I Brook 2004 Microbiology and management of peritonsillar, retropharyngeal, and parapharyngeal abscesses J Oral Maxillofac Surg 62 1545 1550.

    • Search Google Scholar
    • Export Citation
  • 12. AE Zautner 2012 Adenotonsillar disease Recent Pat Inflamm Allergy Drug Discov 6 121 129.

  • 13. RJ Gaffney MT Cafferkey 1988 Bacteriology of normal and diseased tonsils assessed by fine-needle aspiration: Haemophilus influenzae and the pathogenesis of recurrent acute tonsillitis Clin Otolaryngol Allied Sci 23 181 185.

    • Search Google Scholar
    • Export Citation
  • 14. JH Jeong DW Lee RA Ryu YS Lee SH Lee JO Kang K Tae 2007 Bacteriologic comparison of tonsil core in recurrent tonsillitis and tonsillar hypertrophy Laryngoscope 117 2146 2151.

    • Search Google Scholar
    • Export Citation
  • 15. UK Griffiths A Clark B Gessner A Miners C Sanderson ER Sedyaningsih KE Mulholland 2012 Dose-specific efficacy of Haemophilus influenzae type b conjugate vaccines: a systematic review and meta-analysis of controlled clinical trials Epidemiol Infect 140 1343 1355.

    • Search Google Scholar
    • Export Citation
  • 16. JA Garcia-Rodriguez MJ Fresnadillo Martinez 2002 Dynamics of nasopharyngeal colonization of potential respiratory pathogens J Antimicrob Chemother 50 S2 59 73.

    • Search Google Scholar
    • Export Citation
  • 17. M Kilian K Poulsen H Lomholt 2002 Evolution of the paralogous hap and iga genes in Haemophilus influenza: evidence for a conserved hap pseudogene associated with microcolony formation in the recently diverged Haemophilus aegyptius and H. influenzae biogroup aegyptius Mol Microbiol 46 1367 1380.

    • Search Google Scholar
    • Export Citation
  • 18. C Darras-Joly O Lortholary JL Mainardi J Etienne L ai]Guillevin J Acar 1997 Haemophilus endocarditis: report of 42 cases in adults and review. Haemophilus Endocarditis Study Group Clin Infect Dis 24 1087 1094.

    • Search Google Scholar
    • Export Citation
  • 19. R Anderson X Wang EC Briere LS Katz AC Cohn TA Clark NE Messonnier LW Mayer 2012 Haemophilus haemolyticus causing clinical disease J Clin Microbiol 50 2462 2465.

    • Search Google Scholar
    • Export Citation
  • 20. M Hotomi M Kono A Togawa J Arai S Takai Y Ikeda M ai]Ogami TF Murphy N Yamanaka 2010 Haemophilus influenzae and Haemophilus haemolyticus in tonsillar cultures of adults with acute pharyngotonsillitis Auris Nasus Larynx 37 594 600.

    • Search Google Scholar
    • Export Citation
  • 21. D Munkundan Z Ecevit M Patel CF Marrs JR Gilsdorf 2007 Pharyngeal colonization dynamics of Haemophilus influenzae and Haemophilus haemolyticus in healthy adult carriers J Clin Microbiol 45 3207 3217.

    • Search Google Scholar
    • Export Citation
  • 22. TF Murphy AL Brauer S Sethi M Kilian X Cai AJ Lesse 2007 Haemophilus haemolyticus: a human respiratory tract commensal to be distinguished from Haemophilus influenzae J Infect Dis 195 81 89.

    • Search Google Scholar
    • Export Citation
  • 23. G Barbé M Babolat JM Boeufgras D Monget J Freney 1994 Evaluation of API NH, a new 2-hour system for identification of Neisseria and Haemophilus species and Moraxella catarrhalis in a routine clinical laboratory J Clin Microbiol 32 187 189.

    • Search Google Scholar
    • Export Citation
  • 24. EL Munson GV Doern 2007 Comparison of three commercial test systems for biotyping Haemophilus influenzae and Haemophilus parainfluenzae J Clin Microbiol 45 4051 4053.

    • Search Google Scholar
    • Export Citation
  • 25. RP Rennie C Brosnikoff S Shokoples LB Reller S Mirrett W Janda K Ristow A Krilcich 2008 Multicenter evaluation of the new Vitek 2 Neisseria-Haemophilus identification card J Clin Microbiol 46 2681 2685.

    • Search Google Scholar
    • Export Citation
  • 26. G Valenza C Ruoff U Vogel M Frosch M Abele-Horn 2007 Microbiological evaluation of the new VITEK 2 Neisseria-Haemophilus identification card J Clin Microbiol 45 3493 3497.

    • Search Google Scholar
    • Export Citation
  • 27. H Frickmann M Christner M Donat A Berger A Essig A Podbielski RM Hagen S Poppert 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.

    • Search Google Scholar
    • Export Citation
  • 28. M Pittman 1953 A classification of the hemolytic bacteria of the genus Haemophilus: Haemophilus haemolyticus Bergey et al. and Haemophilus parahaemolyticus nov spec J Bacteriol 65 750 751.

    • Search Google Scholar
    • Export Citation
  • 29. KW McCrea J Xie N LaCross M Patel D Mukundan TF Murphy CF Marrs JR Gilsdorf 2008 Relationships of nontypeable Haemophilus influenzae strains to hemolytic and non-hemolytic Haemophilus haemolyticus strains J Clin Microbiol 46 406 416.

    • Search Google Scholar
    • Export Citation
  • 30. PA Totten DV Norn WE Stamm 1995 Characterization of the hemolytic activity of Haemophilus ducreyi Infect Immun 63 4409 4416.

  • 31. N Nørskov-Lauritsen MD Overballe M Kilian 2009 Delineation of the species Haemophilus influenzae by phenotype, multilocus sequence phylogeny, and detection of marker genes J Bacteriol 191 822 831.

    • Search Google Scholar
    • Export Citation
  • 32. E Munson M Pfaller F Koontz G Doern 2002 Comparison of porphyrin-based, growth factor-based, and biochemicalbased testing methods for identification of Haemophilus influenzae Eur J Clin Microbiol Infect Dis 21 196 203.

    • Search Google Scholar
    • Export Citation
  • 33. LAS Kirkham SP Wiertsema EN Mowe JM Bowman TV Riley PC Richmond 2010 Nasopharyngeal carriage of Haemophilus haemolyticus in otitis-prone and healthy children J Clin Microbiol 48 2557 2559.

    • Search Google Scholar
    • Export Citation
  • 34. C Clopper ES Pearson 1934 The use of confidence or fiducial limits illustrated in the case of the binomial Biometrika 26 404 413.

  • 35. A Agresti A Coull 1998 Approximate is better than “exact” for interval estimation of binomial Proportions American Statistician 52 119 126.

    • Search Google Scholar
    • Export Citation
  • 36. S Dommerich H Frickmann J Ostwald T Lindner AE Zautner K Arndt HW Pau A Podbielski 2012 Effects of high hydrostatic pressure on bacterial growth on human ossicles explanted from cholesteatoma patients PLoS One 7 e30150.

    • Search Google Scholar
    • Export Citation
  • 37. H Faden L Duffy A Williams DA Krystofik J Wolf 1995 Epidemiology of nasopharyngeal colonization with non-typeable Haemophilus influenzae in the first 2 years of life J Infect Dis 172 132 135.

    • Search Google Scholar
    • Export Citation

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