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The presence of biofilm-producing bacteria on tonsils is associated with increased exhaled nitric oxide levels: preliminary data in children who experience recurrent exacerbations of chronic tonsillitis

Published online by Cambridge University Press:  06 February 2015

S Torretta ,
P Marchisio ,
L Drago ,
P Capaccio ,
E Baggi  and
L Pignataro
S Torretta*
Affiliation:
Department of Clinical Sciences and Community Health, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
P Marchisio
Affiliation:
Department of Physiopathology and Transplantations, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
L Drago
Affiliation:
Clinical Chemistry and Microbiology Laboratory, IRCCS Galeazzi Hospital and Laboratory of Microbiology and Technological Sciences for Laboratory Medicine, Department of Biomedical Sciences for Health, Università degli Studi di Milano, Italy
P Capaccio
Affiliation:
Department of Surgical and Dental Biomedical Sciences, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
E Baggi
Affiliation:
Department of Physiopathology and Transplantations, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
L Pignataro
Affiliation:
Department of Clinical Sciences and Community Health, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
*
Address for correspondence: Dr Sara Torretta, Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico, Via F. Sforza 35, 20122 Milano, Italy Fax:+39 0250320248 E-mail: [email protected]
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Abstract

Background:

It has been suggested that bacterial biofilms may be a causative factor in the aetiopathogenesis of chronic tonsillitis. Involvement of exhaled nitric oxide has been previously considered, with conflicting findings.

Objective:

A pilot study was performed to investigate the relationship between exhaled nitric oxide levels and the presence of tonsillar biofilm-producing bacteria in children with chronic tonsillitis.

Method:

Tonsillar biofilm-producing bacteria on bioptic specimens taken during tonsillectomy were assessed by means of spectrophotometry.

Results:

Analysis was based on 24 children aged 5–10 years (median, 7.5 years). Biofilm-producing bacteria were found in 40.9 per cent of specimens. The median exhaled nitric oxide level was 11.6 ppb (range, 3.2–22.3 ppb). There was a significant relationship between the presence of biofilm-producing bacteria and increased exhaled nitric oxide levels (p = 0.03). Children with exhaled nitric oxide levels of more than 8 ppb were at three times greater risk of developing tonsillar biofilm-producing bacteria than those with lower levels.

Conclusion:

Our findings suggest the possibility of discriminating children with chronic biofilm-sustained tonsillar infections on the basis of exhaled nitric oxide levels.

Keywords

BiofilmTonsillitisNitric OxideChildren
Type
Main Articles
Information
The Journal of Laryngology & Otology , Volume 129 , Issue 3 , March 2015 , pp. 267 - 272
Copyright
Copyright © JLO (1984) Limited 2015 

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References

1Chole, RA, Faddis, BT. Anatomical evidence of microbial biofilms in tonsillar tissues: a possible mechanism to explain chronicity. Arch Otolaryngol Head Neck Surg 2003;129:634–6Google Scholar
2Al-Mazrou, KA, Al-Khattaf, AS. Adherent biofilms in adenotonsillar diseases in children. Arch Otolaryngol Head Neck Surg 2008;134:20–3CrossRefGoogle ScholarPubMed
3Kasperska-Zajac, A, Czecior, E, Namyslowski, G. Effect of tonsillectomy on the level of exhaled nitric oxide (NO) in patients with recurrent tonsillitis. Respir Med 2010;104:1757–9CrossRefGoogle ScholarPubMed
4Unal, M, Cimen, MY, Doğruer, ZN, Cevik, T. The potential inflammatory role of arginase and iNOS in children with chronic adenotonsillar hypertrophy. Int J Pediatr Otorhinolaryngol 2005;69:381–5CrossRefGoogle ScholarPubMed
5Post, JC, Stoodley, P, Hall-Stoodley, L, Ehrlich, GD. The role of biofilms in otolaryngologic infections. Curr Opin Otolaryngol Head Neck Surg 2004;12:185–90CrossRefGoogle ScholarPubMed
6Galli, J, Calò, L, Ardito, F, Imperiali, M, Bassotti, E, Fadda, G et al. Biofilm formation by Haemophilus influenzae isolated from adeno-tonsil tissue samples, and its role in recurrent adenotonsillitis. Acta Otorhinolaryngol Ital 2007;27:134–8Google Scholar
7Wang, HW, Su, WF, Lin, YS, Kang, BH. Immunolocalization of inducible nitric oxide synthase and 3-nitrotyrosine in recurrently inflamed, human palatine tonsils. Eur Arch Otorhinolaryngol 2002;259:413–18CrossRefGoogle ScholarPubMed
8Kasperska-Zajac, A, Brzoza, Z, Czecior, E, Rogala, B, Polok, A, Namyslowski, G. Elevated levels of exhaled nitric oxide in recurrent tonsillitis. Eur Respir J 2008;31:909–10CrossRefGoogle ScholarPubMed
9Torretta, S, Marchisio, P, Esposito, S, Garavello, W, Cappadona, M, Clemente, IA et al. Exhaled nitric oxide levels in children with chronic adenotonsillar disease. Int J Immunopathol Pharmacol 2011;24:471–80CrossRefGoogle ScholarPubMed
10Baraldi, E, de Jongste, JC; European Respiratory Society /American Thoracic Society (ERS/ATS) Task Force. Measurement of exhaled nitric oxide in children, 2001. Eur Respir J 2002;20:223–37Google Scholar
11Paradise, JL, Bluestone, CD, Bachman, RZ, Colborn, DK, Bernard, BS, Taylor, FH et al. Efficacy of tonsillectomy for recurrent throat infection in severely affected children: results of parallel randomized and nonrandomized clinical trials. N Engl J Med 1984;310:674–83Google Scholar
12Christensen, GD, Simpson, WA, Younger, JJ. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 1985;22:996–1006CrossRefGoogle ScholarPubMed
13Torretta, S, Drago, L, Marchisio, P, Cappadona, M, Rinaldi, V, Nazzari, E et al. Recurrences in chronic tonsillitis substained by tonsillar biofilm-producing bacteria in children. Relationship with the grade of tonsillar hyperplasy. Int J Pediatr Otorhinolaryngol 2013;77:200–4CrossRefGoogle ScholarPubMed
14Torretta, S, Drago, L, Marchisio, P, Gaffuri, M, Clemente, IA, Pignataro, L. Topographic distribution of biofilm-producing bacteria in adenoid subsites of children with chronic or recurrent middle ear infections. Ann Otol Rhinol Laryngol 2013;122:109–13Google Scholar
15Drago, L, De Vecchi, E, Torretta, S, Mattina, R, Marchisio, P, Pignataro, L. Biofilm formation by bacteria isolated from upper respiratory tract before and after adenotonsillectomy. APMIS 2012;120:410–16Google Scholar
16Torretta, S, Marchisio, P, Drago, L, Baggi, E, De Vecchi, E, Garavello, W et al. Nasopharyngeal biofilm-producing otopathogens in children with nonsevere recurrent acute otitis media. Otolaryngol Head Neck Surg 2012;146:991–6Google Scholar
17Torretta, S, Drago, L, Marchisio, P, Mattina, R, Clemente, IA, Pignataro, L. Diagnostic accuracy of nasopharyngeal swabs in detecting biofilm-producing bacteria in chronic adenoiditis: a preliminary study. Otolaryngol Head Neck Surg 2011;144:784–8Google Scholar
18Buchvald, F, Baraldi, E, Carraro, S, Gaston, B, De Jongste, J, Pijnenburg, MW et al. Measurements of exhaled nitric oxide in healthy subjects age 4 to 17 years. J Allergy Clin Immunol 2005;115:1130–6Google Scholar
19Malmberg, LP, Petäys, T, Haahtela, T, Laatikainen, T, Jousilahti, P, Vartiainen, E et al. Exhaled nitric oxide in healthy nonatopic school-age children: determinants and height-adjusted reference values. Pediatr Pulmonol 2006;41:635–42Google Scholar
20Schreiber, F, Beutler, M, Enning, D, Lamprecht-Grandio, M, Zafra, O, González-Pastor, JE et al. The role of nitric-oxide-synthase-derived nitric oxide in multicellular traits of Bacillus subtilis 3610: biofilm formation, swarming, and dispersal. BMC Microbiol 2011;11:111CrossRefGoogle ScholarPubMed
21Schreiber, F, Loeffler, B, Polerecky, L, Kuypers, MM, de Beer, D. Mechanisms of transient nitric oxide and nitrous oxide production in a complex biofilm. ISME J 2009;3:1301–13Google Scholar
22Barraud, N, Schleheck, D, Klebensberger, J, Webb, JS, Hassett, DJ, Rice, SA et al. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 2009;191:7333–42Google Scholar
23Falsetta, ML, McEwan, AG, Jennings, MP, Apicella, MA. Anaerobic metabolism occurs in the substratum of gonococcal biofilms and may be sustained in part by nitric oxide. Infect Immun 2010;78:2320–8Google Scholar
24Alderton, WK, Cooper, CE, Knowles, RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001;357:593–615Google Scholar
25Sudhamsu, J, Crane, BR. Bacterial nitric oxide synthases: what are they good for? Trends Microbiol 2009;17:212–18Google Scholar
26Stamler, JS, Lamas, S, Fang, FC. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 2001;106:675–83Google Scholar
27Gusarov, I, Shatalin, K, Starodubtseva, M, Nudler, E. Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 2009;325:1380–4CrossRefGoogle ScholarPubMed
28Smith, A, Buchinsky, FJ, Post, CJ. Eradicating chronic ear, nose, and throat infections: a systematically conducted literature review of advances in biofilm treatment. Otolaryngol Head Neck Surg 2011;144:338–47Google Scholar