Skip to main content

Advertisement

Log in

Role of biofilm in children with recurrent upper respiratory tract infections

  • Review
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Recurrent respiratory tract infections (RRTIs) are very common in children and a major challenge for pediatricians. In the last few years, bacterial biofilms have been linked to RRTIs and antibiotic resistance, and have raised serious concerns regarding the therapeutic management of recurrent middle ear diseases, chronic rhinosinusitis, and recurrent pharyngotonsillitis. This paper aims to review the new insights into biofilm-related upper respiratory tract infections in children and possible therapeutic strategies. It focuses on the clinical implications for recurrent disease and on studies in pediatric patients. Analysis of the literature showed that the involvement of bacterial biofilm in recurrent upper airway tract infections is an emerging problem that may lead to serious concerns about infection control. Despite the large amount of research within this field, detailed insight into the complex structure of bacterial biofilms and the ultrastructural and biochemical mechanisms responsible for its evasion of the immune system and resistance to treatments is currently lacking. In the future, additional emphasis should be placed on biofilm management as a component of therapeutic strategies. This goal can be attained by finding feasible methods for detecting biofilms in vivo and identifying effective methods for administering treatments that eradicate preexisting bacterial biofilms or hinder bacterial adhesion to respiratory cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Principi N, Esposito S, Cavagna R, Bosis S, Droghetti R, Faelli N, Tosi S, Begliatti E; Snoopy Study Group (2003) Recurrent respiratory tract infections in pediatric age: a population-based survey of the therapeutic role of macrolides. J Chemother 15:53–59

    CAS  PubMed  Google Scholar 

  2. Marchisio P, Bellussi L, Di Mauro G, Doria M, Felisati G, Longhi R, Novelli A, Speciale A, Mansi N, Principi N (2010) Acute otitis media: from diagnosis to prevention. Summary of the Italian guideline. Int J Pediatr Otorhinolaryngol 74:1209–1216

    PubMed  Google Scholar 

  3. Esposito S, Principi N; Italian Society of Pediatrics; Italian Society of Pediatric Infectivology; Italian Society of Pediatric Allergology and Immunology; Italian Society of Pediatric Respiratory Diseases; Italian Society of Preventive and Social Pediatrics; Italian Society of Otorhinolaryngology; Italian Society of Chemotherapy; Italian Society of Microbiology (2008) Guidelines for the diagnosis and treatment of acute and subacute rhinosinusitis in children. J Chemother 20:147–157

    CAS  PubMed  Google Scholar 

  4. Bellussi LM, Marchisio P, Materia E, Passàli FM (2011) Clinical guideline on adenotonsillectomy: the Italian experience. Adv Otorhinolaryngol 72:142–145

    PubMed  Google Scholar 

  5. Esposito S, Musio A (2013) Immunostimulants and prevention of recurrent respiratory tract infections. J Biol Regul Homeost Agents 27:627–636

    CAS  PubMed  Google Scholar 

  6. Esposito S, Marchisio P, Cavagna R, Gironi S, Bosis S, Lambertini L, Droghetti R, Principi N (2003) Effectiveness of influenza vaccination of children with recurrent respiratory tract infections in reducing respiratory-related morbidity within the households. Vaccine 21:3162–3168

    PubMed  Google Scholar 

  7. de Martino M, Ballotti S (2007) The child with recurrent respiratory infections: normal or not? Pediatr Allergy Immunol 18(Suppl 18):13–18

    PubMed  Google Scholar 

  8. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    CAS  PubMed  Google Scholar 

  9. Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122

    CAS  PubMed  Google Scholar 

  10. Vlastarakos PV, Nikolopoulos TP, Maragoudakis P, Tzagaroulakis A, Ferekidis E (2007) Biofilms in ear, nose, and throat infections: how important are they? Laryngoscope 117:668–673

    PubMed  Google Scholar 

  11. Pettigrew MM, Gent JF, Revai K, Patel JA, Chonmaitree T (2008) Microbial interactions during upper respiratory tract infections. Emerg Infect Dis 14:1584–1591

    PubMed Central  PubMed  Google Scholar 

  12. Marks LR, Davidson BA, Knight PR, Hakansson AP (2013) Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease. MBio 4:e00438-13

    PubMed Central  PubMed  Google Scholar 

  13. McCullers JA (2014) The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol 12:252–262. doi:10.1038/nrmicro3231. Epub 2014 Mar 3

    CAS  PubMed  Google Scholar 

  14. Liu YC, Post JC (2009) Biofilms in pediatric respiratory and related infections. Curr Allergy Asthma Rep 9:449–455

    CAS  PubMed  Google Scholar 

  15. Torretta S, Drago L, Marchisio P, Mattina R, Clemente IA, Pignataro L (2011) Diagnostic accuracy of nasopharyngeal swabs in detecting biofilm-producing bacteria in chronic adenoiditis: a preliminary study. Otolaryngol Head Neck Surg 144:784–788

    PubMed  Google Scholar 

  16. Hannig C, Follo M, Hellwig E, Al-Ahmad A (2010) Visualization of adherent micro-organisms using different techniques. J Med Microbiol 59(Pt 1):1–7

    CAS  PubMed  Google Scholar 

  17. Post JC, Stoodley P, Hall-Stoodley L, Ehrlich GD (2004) The role of biofilms in otolaryngologic infections. Curr Opin Otolaryngol Head Neck Surg 12:185–190

    PubMed  Google Scholar 

  18. Post JC, Hiller NL, Nistico L, Stoodley P, Ehrlich GD (2007) The role of biofilms in otolaryngologic infections: update 2007. Curr Opin Otolaryngol Head Neck Surg 15:347–351

    PubMed  Google Scholar 

  19. Gelardi M, Passalacqua G, Fiorella ML, Mosca A, Quaranta N (2011) Nasal cytology: the “infectious spot”, an expression of a morphological-chromatic biofilm. Eur J Clin Microbiol Infect Dis 30:1105–1109

    CAS  PubMed  Google Scholar 

  20. Hoa M, Tomovic S, Nistico L, Hall-Stoodley L, Stoodley P, Sachdeva L, Berk R, Coticchia JM (2009) Identification of adenoid biofilms with middle ear pathogens in otitis-prone children utilizing SEM and FISH. Int J Pediatr Otorhinolaryngol 73:1242–1248

    PubMed  Google Scholar 

  21. Zuliani G, Carlisle M, Duberstein A, Haupert M, Syamal M, Berk R, Du W, Coticchia J (2009) Biofilm density in the pediatric nasopharynx: recurrent acute otitis media versus obstructive sleep apnea. Ann Otol Rhinol Laryngol 118:519–524

    PubMed  Google Scholar 

  22. Hall-Stoodley L, Hu FZ, Gieseke A, Nistico L, Nguyen D, Hayes J, Forbes M, Greenberg DP, Dice B, Burrows A, Wackym PA, Stoodley P, Post JC, Ehrlich GD, Kerschner JE (2006) Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 296:202–211

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Al-Mazrou KA, Al-Khattaf AS (2008) Adherent biofilms in adenotonsillar diseases in children. Arch Otolaryngol Head Neck Surg 134:20–23

    PubMed  Google Scholar 

  24. Homøe P, Bjarnsholt T, Wessman M, Sørensen HC, Johansen HK (2009) Morphological evidence of biofilm formation in Greenlanders with chronic suppurative otitis media. Eur Arch Otorhinolaryngol 266:1533–1538

    PubMed  Google Scholar 

  25. Nistico L, Kreft R, Gieseke A, Coticchia JM, Burrows A, Khampang P, Liu Y, Kerschner JE, Post JC, Lonergan S, Sampath R, Hu FZ, Ehrlich GD, Stoodley P, Hall-Stoodley L (2011) Adenoid reservoir for pathogenic biofilm bacteria. J Clin Microbiol 49:1411–1420

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Bakaletz LO (2012) Bacterial biofilms in the upper airway—evidence for role in pathology and implications for treatment of otitis media. Paediatr Respir Rev 13:154–159

    PubMed Central  PubMed  Google Scholar 

  27. Saafan ME, Ibrahim WS, Tomoum MO (2013) Role of adenoid biofilm in chronic otitis media with effusion in children. Eur Arch Otorhinolaryngol 270:2417–2425

    PubMed  Google Scholar 

  28. Rayner MG, Zhang Y, Gorry MC, Chen Y, Post JC, Ehrlich GD (1998) Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. JAMA 279:296–299

    CAS  PubMed  Google Scholar 

  29. Hoa M, Syamal M, Sachdeva L, Berk R, Coticchia J (2009) Demonstration of nasopharyngeal and middle ear mucosal biofilms in an animal model of acute otitis media. Ann Otol Rhinol Laryngol 118:292–298

    PubMed  Google Scholar 

  30. Moriyama S, Hotomi M, Shimada J, Billal DS, Fujihara K, Yamanaka N (2009) Formation of biofilm by Haemophilus influenzae isolated from pediatric intractable otitis media. Auris Nasus Larynx 36:525–531

    PubMed  Google Scholar 

  31. Yano H, Yamazaki Y, Qin L, Okitsu N, Yahara K, Irimada M, Hirakata Y, Kaku M, Kobayashi T, Watanabe H (2013) Improvement rate of acute otitis media caused by Haemophilus influenzae at 1 week is significantly associated with time to recovery. J Clin Microbiol 51:3542–3546

    PubMed Central  PubMed  Google Scholar 

  32. Mizrahi A, Cohen R, Varon E, Bonacorsi S, Bechet S, Poyart C, Levy C, Raymond J (2014) Non typable-Haemophilus influenzae biofilm formation and acute otitis media. BMC Infect Dis 14:400

    PubMed Central  PubMed  Google Scholar 

  33. García-Cobos S, Moscoso M, Pumarola F, Arroyo M, Lara N, Pérez-Vázquez M, Aracil B, Oteo J, García E, Campos J (2014) Frequent carriage of resistance mechanisms to β-lactams and biofilm formation in Haemophilus influenzae causing treatment failure and recurrent otitis media in young children. J Antimicrob Chemother 69:2394–2399

    PubMed  Google Scholar 

  34. Torretta S, Marchisio P, Drago L, Baggi E, De Vecchi E, Garavello W, Nazzari E, Pignataro L, Esposito S (2012) Nasopharyngeal biofilm-producing otopathogens in children with nonsevere recurrent acute otitis media. Otolaryngol Head Neck Surg 146:991–996

    PubMed  Google Scholar 

  35. Daniel M, Imtiaz-Umer S, Fergie N, Birchall JP, Bayston R (2012) Bacterial involvement in otitis media with effusion. Int J Pediatr Otorhinolaryngol 76:1416–1422

    CAS  PubMed  Google Scholar 

  36. Saylam G, Tatar EC, Tatar I, Ozdek A, Korkmaz H (2010) Association of adenoid surface biofilm formation and chronic otitis media with effusion. Arch Otolaryngol Head Neck Surg 136:550–555

    PubMed  Google Scholar 

  37. Torretta S, Drago L, Marchisio P, Gaffuri M, Clemente IA, Pignataro L (2013) Topographic distribution of biofilm-producing bacteria in adenoid subsites of children with chronic or recurrent middle ear infections. Ann Otol Rhinol Laryngol 122:109–113

    PubMed  Google Scholar 

  38. Chole RA, Faddis BT (2003) Anatomical evidence of microbial biofilms in tonsillar tissues: a possible mechanism to explain chronicity. Arch Otolaryngol Head Neck Surg 129:634–636

    PubMed  Google Scholar 

  39. Galli J, Calò L, Ardito F, Imperiali M, Bassotti E, Fadda G, Paludetti G (2007) Biofilm formation by Haemophilus influenzae isolated from adeno-tonsil tissue samples, and its role in recurrent adenotonsillitis. Acta Otorhinolaryngol Ital 27:134–138

    PubMed Central  CAS  PubMed  Google Scholar 

  40. Stoodley P, Debeer D, Longwell M, Nistico L, Hall-Stoodley L, Wenig B, Krespi YP (2009) Tonsillolith: not just a stone but a living biofilm. Otolaryngol Head Neck Surg 141:316–321

    PubMed  Google Scholar 

  41. Marks LR, Mashburn-Warren L, Federle MJ, Hakansson AP (2014) Streptococcus pyogenes biofilm growth in vitro and in vivo and its role in colonization, virulence, and genetic exchange. J Infect Dis 210:25–34

    PubMed  Google Scholar 

  42. Roberts AL, Connolly KL, Kirse DJ, Evans AK, Poehling KA, Peters TR, Reid SD (2012) Detection of group A Streptococcus in tonsils from pediatric patients reveals high rate of asymptomatic streptococcal carriage. BMC Pediatr 12:3

    PubMed Central  PubMed  Google Scholar 

  43. Ogawa T, Terao Y, Okuni H, Ninomiya K, Sakata H, Ikebe K, Maeda Y, Kawabata S (2011) Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis. Microb Pathog 51:58–68

    CAS  PubMed  Google Scholar 

  44. Brodsky L, Adler E, Stanievich JF (1989) Naso- and oropharyngeal dimensions in children with obstructive sleep apnea. Int J Pediatr Otorhinolaryngol 17:1–11

    CAS  PubMed  Google Scholar 

  45. Torretta S, Drago L, Marchisio P, Cappadona M, Rinaldi V, Nazzari E, Pignataro L (2013) Recurrences in chronic tonsillitis substained by tonsillar biofilm-producing bacteria in children. Relationship with the grade of tonsillar hyperplasy. Int J Pediatr Otorhinolaryngol 77:200–204

    PubMed  Google Scholar 

  46. Starner TD, Zhang N, Kim G, Apicella MA, McCray PB Jr (2006) Haemophilus influenzae forms biofilms on airway epithelia: implications in cystic fibrosis. Am J Respir Crit Care Med 174:213–220

    PubMed Central  PubMed  Google Scholar 

  47. Kasperska-Zajac A, Czecior E, Namyslowski G (2010) Effect of tonsillectomy on the level of exhaled nitric oxide (NO) in patients with recurrent tonsillitis. Respir Med 104:1757–1759

    CAS  PubMed  Google Scholar 

  48. Torretta S, Marchisio P, Esposito S, Garavello W, Cappadona M, Clemente IA, Pignataro L (2011) Exhaled nitric oxide levels in children with chronic adenotonsillar disease. Int J Immunopathol Pharmacol 24:471–480

    CAS  PubMed  Google Scholar 

  49. Schreiber F, Beutler M, Enning D, Lamprecht-Grandio M, Zafra O, González-Pastor JE, de Beer D (2011) The role of nitric-oxide-synthase-derived nitric oxide in multicellular traits of Bacillus subtilis 3610: biofilm formation, swarming, and dispersal. BMC Microbiol 11:111

    PubMed Central  CAS  PubMed  Google Scholar 

  50. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191:7333–7342

    PubMed Central  CAS  PubMed  Google Scholar 

  51. Falsetta ML, McEwan AG, Jennings MP, Apicella MA (2010) Anaerobic metabolism occurs in the substratum of gonococcal biofilms and may be sustained in part by nitric oxide. Infect Immun 78:2320–2328

    PubMed Central  CAS  PubMed  Google Scholar 

  52. Jardeleza C, Foreman A, Baker L, Paramasivan S, Field J, Tan LW, Wormald PJ (2011) The effects of nitric oxide on Staphylococcus aureus biofilm growth and its implications in chronic rhinosinusitis. Int Forum Allergy Rhinol 1:438–444

    PubMed  Google Scholar 

  53. Sudhamsu J, Crane BR (2009) Bacterial nitric oxide synthases: what are they good for? Trends Microbiol 17:212–218

    CAS  PubMed  Google Scholar 

  54. Esposito S, Marchisio P, Tenconi R, Tagliaferri L, Albertario G, Patria MF, Principi N (2012) Diagnosis of acute rhinosinusitis. Pediatr Allergy Immunol 23(Suppl 22):17–19

    PubMed  Google Scholar 

  55. Chow AW, Benninger MS, Brook I, Brozek JL, Goldstein EJ, Hicks LA, Pankey GA, Seleznick M, Volturo G, Wald ER, File TM Jr; Infectious Diseases Society of America (2012) IDSA clinical practice guideline for acute bacterial rhinosinusitis in children and adults. Clin Infect Dis 54:1041–1045

    CAS  Google Scholar 

  56. Silviu-Dan F (2011) Pediatric chronic rhinosinusitis: the old, the new, and the reasonable. Pediatr Ann 40:213–220

    PubMed  Google Scholar 

  57. Akdis CA, Bachert C, Cingi C, Dykewicz MS, Hellings PW, Naclerio RM, Schleimer RP, Ledford D (2013) Endotypes and phenotypes of chronic rhinosinusitis: a PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol 131:1479–1490

    PubMed Central  PubMed  Google Scholar 

  58. Perloff JR, Palmer JN (2005) Evidence of bacterial biofilms in a rabbit model of sinusitis. Am J Rhinol 19:1–6

    PubMed  Google Scholar 

  59. Sanclement JA, Webster P, Thomas J, Ramadan HH (2005) Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope 115:578–582

    PubMed  Google Scholar 

  60. Hunsaker DH, Leid JG (2008) The relationship of biofilms to chronic rhinosinusitis. Curr Opin Otolaryngol Head Neck Surg 16:237–241

    PubMed  Google Scholar 

  61. Ramadan HH, Sanclement JA, Thomas JG (2005) Chronic rhinosinusitis and biofilms. Otolaryngol Head Neck Surg 132:414–417

    PubMed  Google Scholar 

  62. Tatar EÇ, Tatar I, Ocal B, Korkmaz H, Saylam G, Ozdek A, Celik HH (2012) Prevalence of biofilms and their response to medical treatment in chronic rhinosinusitis without polyps. Otolaryngol Head Neck Surg 146:669–675

    PubMed  Google Scholar 

  63. Chen HH, Liu X, Ni C, Lu YP, Xiong GY, Lu YY, Wang SQ (2012) Bacterial biofilms in chronic rhinosinusitis and their relationship with inflammation severity. Auris Nasus Larynx 39:169–174

    CAS  PubMed  Google Scholar 

  64. Ragab A, Essa N, El-Raghy N, Zahran W, El Borolsy A (2012) Evaluation of bacterial adherence and biofilm arrangements as new targets in treatment of chronic rhinosinusitis. Eur Arch Otorhinolaryngol 269:537–544

    PubMed  Google Scholar 

  65. Foreman A, Boase S, Psaltis A, Wormald PJ (2012) Role of bacterial and fungal biofilms in chronic rhinosinusitis. Curr Allergy Asthma Rep 12:127–135

    PubMed  Google Scholar 

  66. Sanderson AR, Leid JG, Hunsaker D (2006) Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope 116:1121–1126

    PubMed  Google Scholar 

  67. Healy DY, Leid JG, Sanderson AR, Hunsaker DH (2008) Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg 138:641–647

    PubMed  Google Scholar 

  68. Mladina R, Skitarelić N, Musić S, Ristić M (2010) A biofilm exists on healthy mucosa of the paranasal sinuses: a prospectively performed, blinded, scanning electron microscope study. Clin Otolaryngol 35:104–110

    CAS  PubMed  Google Scholar 

  69. Li H, Wang D, Sun X, Hu L, Yu H, Wang J (2012) Relationship between bacterial biofilm and clinical features of patients with chronic rhinosinusitis. Eur Arch Otorhinolaryngol 269:155–163

    PubMed  Google Scholar 

  70. Bendouah Z, Barbeau J, Hamad WA, Desrosiers M (2006) Biofilm formation by Staphylococcus aureus and Pseudomonas aeruginosa is associated with an unfavorable evolution after surgery for chronic sinusitis and nasal polyposis. Otolaryngol Head Neck Surg 134:991–996

    PubMed  Google Scholar 

  71. Singhal D, Psaltis AJ, Foreman A, Wormald PJ (2010) The impact of biofilms on outcomes after endoscopic sinus surgery. Am J Rhinol Allergy 24:169–174

    PubMed  Google Scholar 

  72. Psaltis AJ, Ha KR, Beule AG, Tan LW, Wormald PJ (2007) Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 117:1302–1306

    PubMed  Google Scholar 

  73. Prince AA, Steiger JD, Khalid AN, Dogrhamji L, Reger C, Eau Claire S, Chiu AG, Kennedy DW, Palmer JN, Cohen NA (2008) Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am J Rhinol 22:239–245

    PubMed  Google Scholar 

  74. Coticchia J, Zuliani G, Coleman C, Carron M, Gurrola J 2nd, Haupert M, Berk R (2007) Biofilm surface area in the pediatric nasopharynx: chronic rhinosinusitis vs obstructive sleep apnea. Arch Otolaryngol Head Neck Surg 133:110–114

    PubMed  Google Scholar 

  75. Zuliani G, Carron M, Gurrola J, Coleman C, Haupert M, Berk R, Coticchia J (2006) Identification of adenoid biofilms in chronic rhinosinusitis. Int J Pediatr Otorhinolaryngol 70:1613–1617

    PubMed  Google Scholar 

  76. Sanchez CJ, Kumar N, Lizcano A, Shivshankar P, Dunning Hotopp JC, Jorgensen JH, Tettelin H, Orihuela CJ (2011) Streptococcus pneumoniae in biofilms are unable to cause invasive disease due to altered virulence determinant production. PLoS One 6:e28738

    PubMed Central  CAS  PubMed  Google Scholar 

  77. Weimer KE, Armbruster CE, Juneau RA, Hong W, Pang B, Swords WE (2010) Coinfection with Haemophilus influenzae promotes pneumococcal biofilm formation during experimental otitis media and impedes the progression of pneumococcal disease. J Infect Dis 202:1068–1075

    PubMed Central  PubMed  Google Scholar 

  78. Ferguson BJ, Stolz DB (2005) Demonstration of biofilm in human bacterial chronic rhinosinusitis. Am J Rhinol 19:452–457

    PubMed  Google Scholar 

  79. Al-Mutairi D, Kilty SJ (2011) Bacterial biofilms and the pathophysiology of chronic rhinosinusitis. Curr Opin Allergy Clin Immunol 11:18–23

    PubMed  Google Scholar 

  80. Karosi T, Sziklai I, Csomor P (2013) Low-frequency ultrasound for biofilm disruption in chronic rhinosinusitis with nasal polyposis: in vitro pilot study. Laryngoscope 123:17–23

    PubMed  Google Scholar 

  81. Drago L, De Vecchi E, Torretta S, Mattina R, Marchisio P, Pignataro L (2012) Biofilm formation by bacteria isolated from upper respiratory tract before and after adenotonsillectomy. APMIS 120:410–416

    PubMed  Google Scholar 

  82. Stewart PS (2014) Biophysics of biofilm infection. Pathog Dis 70:212–218

    CAS  PubMed  Google Scholar 

  83. Macià MD, Rojo-Molinero E, Oliver A (2014) Antimicrobial susceptibility testing in biofilm-growing bacteria. Clin Microbiol Infect. Epub 2014 Apr 26

  84. Smith A, Buchinsky FJ, Post JC (2011) Eradicating chronic ear, nose, and throat infections: a systematically conducted literature review of advances in biofilm treatment. Otolaryngol Head Neck Surg 144:338–347

    PubMed  Google Scholar 

  85. Desrosiers M, Bendouah Z, Barbeau J (2007) Effectiveness of topical antibiotics on Staphylococcus aureus biofilm in vitro. Am J Rhinol 21:149–153

    PubMed  Google Scholar 

  86. Solares CA, Batra PS, Hall GS, Citardi MJ (2006) Treatment of chronic rhinosinusitis exacerbations due to methicillin-resistant Staphylococcus aureus with mupirocin irrigations. Am J Otolaryngol 27:161–165

    CAS  PubMed  Google Scholar 

  87. Oxley KS, Thomas JG, Ramadan HH (2007) Effect of ototopical medications on tympanostomy tube biofilms. Laryngoscope 117:1819–1824

    CAS  PubMed  Google Scholar 

  88. Wang JC, Hamood AN, Saadeh C, Cunningham MJ, Yim MT, Cordero J (2014) Strategies to prevent biofilm-based tympanostomy tube infections. Int J Pediatr Otorhinolaryngol 78:1433–1438

    PubMed  Google Scholar 

  89. Kim SG, Yoon YH, Choi JW, Rha KS, Park YH (2012) Effect of furanone on experimentally induced Pseudomonas aeruginosa biofilm formation: in vitro study. Int J Pediatr Otorhinolaryngol 76:1575–1578

    PubMed  Google Scholar 

  90. Steel HC, Theron AJ, Cockeran R, Anderson R, Feldman C (2012) Pathogen- and host-directed anti-inflammatory activities of macrolide antibiotics. Mediators Inflamm 2012:584262

    PubMed Central  PubMed  Google Scholar 

  91. Singhal D, Jekle A, Debabov D, Wang L, Khosrovi B, Anderson M, Foreman A, Wormald PJ (2012) Efficacy of NVC-422 against Staphylococcus aureus biofilms in a sheep biofilm model of sinusitis. Int Forum Allergy Rhinol 2:309–315

    PubMed  Google Scholar 

  92. Korkmaz H, Ocal B, Tatar EC, Tatar I, Ozdek A, Saylam G, Celik HH (2014) Biofilms in chronic rhinosinusitis with polyps: is eradication possible? Eur Arch Otorhinolaryngol 271:2695–2702

    PubMed  Google Scholar 

  93. Chen K, Wu X, Jiang G, Du J, Jiang H (2013) Low dose macrolide administration for long term is effective for otitis media with effusion in children. Auris Nasus Larynx 40:46–50

    PubMed  Google Scholar 

  94. Kilty SJ, Duval M, Chan FT, Ferris W, Slinger R (2011) Methylglyoxal: (active agent of manuka honey) in vitro activity against bacterial biofilms. Int Forum Allergy Rhinol 1:348–350

    PubMed  Google Scholar 

  95. Drago L, Cappelletti L, De Vecchi E, Pignataro L, Torretta S, Mattina R (2014) Antiadhesive and antibiofilm activity of hyaluronic acid against bacteria responsible for respiratory tract infections. APMIS 122:1013–1019

    CAS  PubMed  Google Scholar 

  96. Riise GC, Qvarfordt I, Larsson S, Eliasson V, Andersson BA (2000) Inhibitory effect of N-acetylcysteine on adherence of Streptococcus pneumoniae and Haemophilus influenzae to human oropharyngeal epithelial cells in vitro. Respiration 67:552–558

    CAS  PubMed  Google Scholar 

  97. Zhao T, Liu Y (2010) N-acetylcysteine inhibit biofilms produced by Pseudomonas aeruginosa. BMC Microbiol 10:140

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Pintucci JP, Corno S, Garotta M (2010) Biofilms and infections of the upper respiratory tract. Eur Rev Med Pharmacol Sci 14:683–690

    CAS  PubMed  Google Scholar 

  99. Marchese A, Debbia EA, Tonoli E, Gualco L, Schito AM (2002) In vitro activity of thiamphenicol against multiresistant Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus in Italy. J Chemother 14:554–561

    CAS  PubMed  Google Scholar 

  100. Macchi A, Ardito F, Marchese A, Schito GC, Fadda G (2006) Efficacy of N-acetyl-cysteine in combination with thiamphenicol in sequential (intramuscular/aerosol) therapy of upper respiratory tract infections even when sustained by bacterial biofilms. J Chemother 18:507–513

    CAS  PubMed  Google Scholar 

  101. Macchi A, Castelnuovo P (2009) Aerosol antibiotic therapy in children with chronic upper airway infections: a potential alternative to surgery. Int J Immunopathol Pharmacol 22:303–310

    CAS  PubMed  Google Scholar 

  102. Varricchio A, Capasso M, Di Gioacchino M, Ciprandi G (2008) Inhaled thiamphenicol and acetylcysteine in children with acute bacterial rhinopharyngitis. Int J Immunopathol Pharmacol 21:625–629

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are financially supported by Bando Giovani Ricercatori 2009 (Italian Ministry of Health).

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Esposito.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nazzari, E., Torretta, S., Pignataro, L. et al. Role of biofilm in children with recurrent upper respiratory tract infections. Eur J Clin Microbiol Infect Dis 34, 421–429 (2015). https://doi.org/10.1007/s10096-014-2261-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-014-2261-1

Keywords

Navigation