Abstract
Introduction. Haemophilus influenzae and Haemophilus parainfluenzae are known as human-restricted respiratory microbiota representatives. The aim of the present paper was to assay haemophili prevalence in middle ear effusion specimens in pediatric patients with otitis media with effusion (OME).
Methods. A total of 86 ear effusion specimens (from the left and right ear independently) were collected from 43 pediatric patients with OME. For comparison, 58 nasopharyngeal specimens were taken from 58 pediatric patients prone to recurrent respiratory tract infections (RRTI). Isolation and identification of haemophili biotypes and antimicrobial susceptibility was accomplished by standard microbiological methods. The cell surface hydrophobicity (CSH) of isolates was assayed by the method of aggregation in ammonium sulfate (SAT).
Results. Haemophili were isolated in 25.6% (11/43) of all OME patients: in 5/43 (11.6%) – H. influenzae (biotypes III, II), in 5/43 (11.6%) – H. parainfluenzae, in 1/43 (2.3%) – both species were found. Haemophili-positive nasopharyngeal specimen was found in 27/58 (46.6%) RRTI patients: in 19/58 (32.8%) – H. influenzae, in 8/58 (13.8%) – H. parainfluenzae. About 90% of all haemophili isolates were characterised by extreme to strong CSH. Antimicrobial resistance occurred mainly among H. parainfluenzae (80%) and to a much lower percentage among H. influenzae (33.3%) isolates. The obtained data suggest that both H. influenzae and H. parainfluenzae can be involved in pathology of OME in pediatric patients. The high cell surface hydrophobicity can affect on the haemophili prevalence and ear colonization, and induces predisposition to the presence of these bacteria as a biofilm that serves as a virulence factor with great importance for the survival of these opportunistic bacteria and their persistence in the ear environment.
References
1. Dhooge IJ. Acute Otitis Media in Children. In: Graham JM, Scadding GK, Bull PD, editors. Pediatric ENT. Heidelberg: Springer;2007: 399-420.
2. Robb PJ. Otitis Media With Effusion. In: Graham JM, Scadding GK, Bull PD, editors. Pediatric ENT. Heidelberg: Springer;2007:413-20.
3. Healy GB, Rosbe KW. Otitis Media and Middle Ear Effusions. In: Snow JB Jr, Ballenger JJ, editors. Ballenger's Otorhinolaryngology Head and Neck Surgery. Hamilton: BC Decker;2003:249-60.
4. Rosenfeld RM, Culpepper L, Doyle KJ. Clinical practice guideline: otitis media with effusion. Otolaryngol Head Neck Surg. 2004;130: 95-118.
5. Saki N, Rahim F, Nikakhlagh S, Sarafraz M, Jafarzadeh E. Quality of life in children with recurrent acute otitis media in southwestern of Iran. Otolar Head and Neck Surg. 2012;66:267-70.
6. Qureishi A, Lee Y, Belfield K, Birchall JP, Daniel M. Update on otitis media – prevention and treatment. Infect Drug Resist. 2014;7:15-24.
7. Tos M . Epidemiology and natural history of secretory otitis. Am J Otol. 1984;5:459-62.
8. Teele DW, Klein JO, Rosner B. Epidemiology of otitis media during the first seven years of life in children in greater Boston: a prospective, cohort study. J Infect Dis. 1989;160:83-94.
9. Minovi A, Dazert S. Diseases of the middle ear in childhood. GMS Curr Top Otorhinolaryngol Head Neck Surg. 2014;13 (11).
10. Bogaert D et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PLoS One. 2011;6: 17035.
11. Massa HM, Cripps AW, Lehmann D. Otitis media: viruses, bacteria, biofilms and vaccines. Med J Aust. 2009;191:44-9.
12. Ngo CC, Massa HM, Thornton RB, Cripps AW. Predominant bacteria detected from the middle ear fluid of children experiencing otitis media: a systematic review. PLoS One. 2016;11:e0150949.
13. Khoramrooz SS et al. Frequency of Alloicoccus otitidis, Streptococcus pneumoniae, Moraxella catarrhalis and Haemophilus influenzae in children with otitis media with effusion (OME) in Iranian patients. Auris Nasus Larynx. 2012;39:369-73.
14. Privitera A et al. Molecular epidemiology and phylogenetic analysis of Haemophilus parainfluenzae from chronic obstructive pulmonary disease exacerbations. Eur J Epidemiol. 1998;14:405-12.
15. Ariza Jiménez AB, Moreno-Perez D, Núñez Cuadros EA. Invasive disease caused by Haemophilus parainfluenzae III in a child with uropathy. J Med Microbiol. 2013;62:792-3.
16. Barkai G, Leibovitz E, Givon-Lavi N, Dagan R. Potential contribution by nontypable Haemophilus influenzae in protracted and recurrent acute otitis media. Pediatr Infect Dis J. 2009;28:466-71.
17. Berndsen MR, Erlendsdóttir H, Gottfredsson M. Evolving epidemiology of invasive Haemophilus infections in the post-vaccination era: results from a long-term population-based study. Clin Microbiol Infect. 2012;18:918-23.
18. Ladhani S, Slack MP, Heath PT, von Gottberg A, Chandra M, Ramsay ME. Invasive Haemophilus influenzae disease, Europe, 1996-2006. Emerging Infect Dis. 2010;16:455-63.
19. Mitchell JL, Hill SL. Immune response to Haemophilus parainfluenzae in patients with chronic obstructive lung disease. Clin Diagn Lab Immunol. 2000;7:25-30.
20. Rele M, Giles M, Daley AJ. Invasive Haemophilus parainfluenzae maternal–infant infections: an Australasian perspective and case report. Aust N Z J Obstet Gynaecol. 2006;46:258-60.
21. Howie VM, Ploussard JH, Lester RL Jr. Otitis media: a clinical and bacteriological correlation. Pediatrics. 1970;45:29-35.
22. Bluestone CD, Stephenson JS, Martin LM. Ten-year review of otitis media pathogens. Pediatr Infect Dis J. 1992;11:7-11.
23. Kilpi T, Herva E, Kaijalainen T, Syrjänen R, Takala AK. Bacteriology of acute otitis media in a cohort of Finnish children followed for the first two years of life. Pediatr Infect Dis J. 2001;20:654-62.
24. Cardines R, Giufrè M, Ciofi degli Atti ML, Accogli M, Mastrantonio P, Cerquetti M. Haemophilus parainfluenzae meningitis in an adult associated with acute otitis media. New Microbiol. 2009;32:213-5.
25. Chonmaitree T, Hendrickson KJ. Detection of respiratory viruses in the middle ear fluids of children with acute otitis media by multiplex reverse transcription-polymerase chain reaction assay. Pediatr Infect Dis J. 2000;19:258-60.
26. Casey JR, Pichichero ME. Changes in frequency and pathogens causing acute otitis media in 1995-2003. Pediatr Infect Dis J. 2004;23: 824-8.
27. Klein JO, Bluestone CD. Otitis media. In: Feigin RD, Cherry JD, Demmler GJ, Kaplan SL, editors. Textbook of pediatric infectious diseases 5. Philadelphia: Saunders;2004:215-35.
28. Goleva et al. The effects of airway microbiome on corticosteroid responsiveness in asthma. Am J Respir Crit Care Med. 2013;188: 1193-201.
29. Faden H et al. Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J Infect Dis. 1997;175:1440-5.
30. Park CW et al. Detection rates of bacteria in chronic otitis media with effusion in children. J K Med Scien. 2004;19:735-8.
31. Watson KC, Kerr EJ, Hinks CA. Distribution of biotypes of Haemophilus influenzae and H. parainfluenzae in patients with cystic fibrosis. J Clin Pathol. 1985;38:750-53.
32. Houang et al. Comparison of genital and respiratory carriage of Haemophilus parainfluenzae in men. J Med Microbiol. 1989;28: 119-23.
33. Martel, AY, St-Laurent G, Dansereau LA, Bergeron MG. Isolation and biochemical characterization of Haemophilus species isolated simultaneously from the oropharyngeal and anogenital areas. J Clin Microbiol. 1989;27:1486-9.
34. Taylor DC et al. Biotypes of Haemophilus parainfluenzae from the respiratory secretions in chronic bronchitis. J Med Microbiol. 1992;36:279-82.
35. Rhind GB, Gould GA, Ahmad F, Croughan MJ, Calder MA. Haemophilus biotypes in respiratory disease. Thorax. 1987;42:151-2.
36. Knobloch JK, Von Osten H, Horstkotte MA, Rohde H, Mack D. Minimal attachment killing (MAK): a versatile method for susceptibility testing of attached biofilm-positive and –negative Staphylococcus epidermidis. Med Microbiol Immunol. 2002;191: 107-14.
37. Zhang XS, Garcia-Contreras R, Wood TK.. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol. 2007;189:3051-62.
38. Das MP. Effect of cell surface hydrophobicity in microbial biofilm formation. Euro J Exp Bio. 2014;4: 254-6.
39. Paluch-Oleś J et al. The phenotypic and genetic biofilm formation characteristics of coagulase-negative staphylococci isolates in children with otitis media. I J of Pediatr Otorhinolar. 2011;75:126-30.
40. Kosikowska et al. Nasopharyngeal and adenoid colonization by Haemophilus influenzae and Haemophilus parainfluenzae in children undergoing adenoidectomy and the ability of bacterial isolates to biofilm production. Medicine. 2015;94:799.
41. Kosikowska et al. Changes in the prevalence and biofilm formation of Haemophilus influenzae and Haemophilus parainfluenzae from the respiratory microbiota of patients with sarcoidosis. BMC Infect Dis. 2016;16:449.
42. Burmolle M, Bahl MI, Jensen LB, Sorensen SJ, Hansen LH. Type 3 fimbriae, encoded by the conjugative plasmid pOLA52, enhance biofilm formation and transfer frequencies in Enterobacteriaceae strains. Microbiol. 2008;154:187-95.
43. Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Inter J Antimicrob Ag. 2010;35: 322-32.
44. Jensen PO, Givskov M, Bjarnsholt T, Moser C. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Mic. 2010;59:292-305.
45. Daniel M, Imtiaz-Umer S, Fergie N, Birchall JP, Bayston R. Bacterial involvement in otitis media with effusion. Int J Pediatr Otorhinolaryngol. 2012;76:1416-22.
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 Unported License.
Copyright (c) 2019 Autors