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Measuring antibiotic levels and their relationship with the microbiome in chronic rhinosinusitis

Published online by Cambridge University Press:  07 October 2019

J Siu Open the ORCID record for J Siu [Opens in a new window] ,
M D Tingle Open the ORCID record for M D Tingle [Opens in a new window]  and
R G Douglas Open the ORCID record for R G Douglas [Opens in a new window]
J Siu
Affiliation:
Department of Surgery, University of Auckland, New Zealand
M D Tingle
Affiliation:
Department of Pharmacology and Clinical Pharmacology, University of Auckland, New Zealand
R G Douglas*
Affiliation:
Department of Surgery, University of Auckland, New Zealand
*
Author for correspondence: Prof Richard George Douglas Department of Surgery, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand E-mail: [email protected] Fax: +64 9 377 9656
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Abstract

Background

The evidence supporting the efficacy of antibiotic therapy in the treatment of chronic rhinosinusitis is not compelling. A limited number of studies show that the changes in the nasal microbiome in patients following drug therapy are unpredictable and variable. The evidence for the impact of oral antibiotics on the gut microbiota is stronger, possibly as a result of differences in drug distribution to various sites around the body. There are few studies on sinus mucosal and mucus levels of oral antibiotics used in the treatment of chronic rhinosinusitis. The distribution dependent effects of antibiotics on the sinonasal microbiome is unclear.

Conclusion

This review highlights that relative drug concentrations and their efficacy on microbiota at different sites is an important subject for future studies investigating chronic rhinosinusitis.

Keywords

BacteriaMicrobiotaSinusitisAntibioticsInflammation
Type
Review Articles
Information
The Journal of Laryngology & Otology , Volume 133 , Issue 10 , October 2019 , pp. 862 - 866
Copyright
Copyright © JLO (1984) Limited, 2019 

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Footnotes

Prof R G Douglas takes responsibility for the integrity of the content of the paper

References

1Wallwork, B, Coman, W, Mackay-Sim, A, Greiff, L, Cervin, A. A double-blind, randomized, placebo-controlled trial of macrolide in the treatment of chronic rhinosinusitis. Laryngoscope 2006;116:189–93Google Scholar
2Stewart, PS, Costerton, JW. Antibiotic resistance of bacteria in biofilms. Lancet 2001;358:135–8Google Scholar
3Kennedy, J, Borish, L. Chronic rhinosinusitis and antibiotics: the good, the bad, and the ugly. Am J Rhinol Allergy 2013;27:467–72Google Scholar
4Zhang, N, Van Zele, T, Perez-Novo, C, Van Bruaene, N, Holtappels, G, DeRuyck, N et al. Different types of T-effector cells orchestrate mucosal inflammation in chronic sinus disease. J Allergy Clin Immunol 2008;122:961–8Google Scholar
5Foreman, A, Holtappels, G, Psaltis, AJ, Jervis-Bardy, J, Field, J, Wormald, PJ et al. Adaptive immune responses in Staphylococcus aureus biofilm-associated chronic rhinosinusitis. Allergy 2011;66:1449–56Google Scholar
6Van Zele, T, Gevaert, P, Holtappels, G, Beule, A, Wormald, PJ, Mayr, S et al. Oral steroids and doxycycline: two different approaches to treat nasal polyps. J Allergy Clin Immunol 2010;125:1069–76.e4Google Scholar
7Hoggard, M, Biswas, K, Zoing, M, Mackenzie B, Wagner, Taylor, MW, Douglas, RG. Evidence of microbiota dysbiosis in chronic rhinosinusitis. Int Forum Allergy Rhinol 2017;7:230–9Google Scholar
8Wagner Mackenzie, B, Waite, DW, Hoggard, M, Douglas, RG, Taylor, MW, Biswas, K. Bacterial community collapse: a meta-analysis of the sinonasal microbiota in chronic rhinosinusitis. Environ Microbiol 2017;19:381–92Google Scholar
9Lee, JT, Frank, DN, Ramakrishnan, V. Microbiome of the paranasal sinuses: update and literature review. Am J Rhinol Allergy 2016;30:3–16Google Scholar
10Antunes, MB, Feldman, MD, Cohen, NA, Chiu, AG. Dose-dependent effects of topical tobramycin in an animal model of Pseudomonas sinusitis. Am J Rhinol Allergy 2007;21:423–7Google Scholar
11Lim, M, Citardi, MJ, Leong, JL. Topical antimicrobials in the management of chronic rhinosinusitis: a systematic review. Am J Rhinol Allergy 2008;22:381–9Google Scholar
12Ha, KR, Psaltis, AJ, Butcher, AR, Wormald, PJ, Tan, LW. In vitro activity of mupirocin on clinical isolates of Staphylococcus aureus and its potential implications in chronic rhinosinusitis. Laryngoscope 2008;118:535–40Google Scholar
13Legent, F, Bordure, P, Beauvillain, C, Berche, P. A double-blind comparison of ciprofloxacin and amoxycillin/clavulanic acid in the treatment of chronic sinusitis. Chemotherapy 1994;40(suppl 1):8–15Google Scholar
14Namyslowski, G, Misiolek, M, Czecior, E, Malafiej, E, Orecka, B, Namyslowski, P et al. Comparison of the efficacy and tolerability of amoxycillin/clavulanic acid 875 mg b.i.d. with cefuroxime 500 mg b.i.d. in the treatment of chronic and acute exacerbation of chronic sinusitis in adults. J Chemother 2002;14:508–17Google Scholar
15Sydnor, TA Jr, Scheld, WM, Gwaltney, J Jr, Nielsen, RW, Huck, W, Therasse, DG. Loracarbef (LY 163892) vs amoxicillin/clavulanate in bacterial maxillary sinusitis. Ear Nose Throat J 1992;71:225–32Google Scholar
16Orlandi, RR, Kingdom, TT, Hwang, PH, Smith, TL, Alt, JA, Baroody, FM et al. International Consensus Statement on Allergy and Rhinology: Rhinosinusitis. Int Forum Allergy Rhinol 2016;6(suppl 1):S22–209Google Scholar
17Suzuki, H, Shimomura, A, Ikeda, K, Furukawa, M, Oshima, T, Takasaka, T. Inhibitory effect of macrolides on interleukin-8 secretion from cultured human nasal epithelial cells. Laryngoscope 1997;107:1661–6Google Scholar
18Pynnonen, MA, Venkatraman, G, Davis, GE. Macrolide therapy for chronic rhinosinusitis: a meta-analysis. Otolaryngol Head Neck Surg 2013;148:366–73Google Scholar
19Ambrose, PG, Anon, JB, Bhavnani, SM, Okusanya, OO, Jones, RN, Paglia, MR et al. Use of pharmacodynamic endpoints for the evaluation of levofloxacin for the treatment of acute maxillary sinusitis. Diagn Microbiol Infect Dis 2008;61:13–2010.1016/j.diagmicrobio.2008.01.010Google Scholar
20Ambrose, PG, Anon, JB, Owen, JS, VanWart, S, McPhee, ME, Bhavnani, SM et al. Use of pharmacodynamic end points in the evaluation of gatifloxacin for the treatment of acute maxillary sinusitis. Clin Infect Dis 2004;38:1513–20Google Scholar
21Axelsson, A, Brorso, JE. Concentration of antibiotics in sinus secretions. Doxycycline and spiramycin. Ann Otol Rhinol Laryngol 1973;82:44–810.1177/000348947308200111Google Scholar
22Cherrier, P, Tod, M, Gros, VL, Petitjean, O, Brion, N, Chatelin, A. Cefotiam concentrations in the sinus fluid of patients with chronic sinusitis after administration of cefotiam hexetil. Eur J Clin Microbiol Infect Dis 1993;12:211–1510.1007/BF01967115Google Scholar
23Dewever, M. Determination of roxithromycin concentration in the mucosa of the maxillary sinus. Br J Clin Pract 1988;42(suppl 55):81Google Scholar
24Dinis, PB, Monteiro, MC, Martins, ML, Silva, N, Morais, JG. Sinus tissue concentration of moxifloxacin after a single oral dose. Ann Otol Rhinol Laryngol 2004;113:142–6Google Scholar
25Dinis, PB, Monteiro, MC, Martins, ML, Silva, N, Gomes, A. Sinus tissue pharmacokinetics after oral administration of amoxicillin/clavulanic acid. Laryngoscope 2000;110:1050–5Google Scholar
26Ehnhage, A, Rautiainen, M, Fang, AF, Sanchez, SP. Pharmacokinetics of azithromycin in serum and sinus fluid after administration of extended-release and immediate-release formulations in patients with acute bacterial sinusitis. Int J Antimicrob Agents 2008;31:561–6Google Scholar
27Eneroth, CM, Lundberg, C, Wretlind, B. Antibiotic concentrations in maxillary sinus secretions and in the sinus mucosa. Chemotherapy 1975;21(suppl 1):1–7Google Scholar
28Fang, AF, Palmer, JN, Chiu, AG, Blumer, JL, Crownover, PH, Campbell, MD et al. Pharmacokinetics of azithromycin in plasma and sinus mucosal tissue following administration of extended-release or immediate-release formulations in adult patients with chronic rhinosinusitis. Int J Antimicrob Agents 2009;34:67–71Google Scholar
29Fraschini, F, Scaglione, F, Pintucci, G, Maccarinelli, G, Dugnani, S, Demartini, G. The diffusion of clarithromycin and roxithromycin into nasal mucosa, tonsil and lung in humans. J Antimicrob Chemother 1991;27(suppl A):61–5Google Scholar
30Gehanno, P, Darantière, S, Dubreuil, C, Chobaut, JC, Bobin, S, Pages, JC et al. A prospective, multicentre study of moxifloxacin concentrations in the sinus mucosa tissue of patients undergoing elective surgery of the sinus. J Antimicrob Chemother 2002;49:821–6Google Scholar
31Gnarpe, H, Lundberg, C. Preliminary report. L-phase organisms in maxillary sinus secretions. Scand J Infect Dis 1971;3:257–9Google Scholar
32Kuehnel, TS, Schurr, C, Lotter, K, Kees, F. Penetration of telithromycin into the nasal mucosa and ethmoid bone of patients undergoing rhinosurgery for chronic sinusitis. J Antimicrob Chemother 2005;44:591–4Google Scholar
33Liss, RH, Norman, JC. Visualization of doxycycline in lung tissue and sinus secretions by fluorescent techniques. Chemotherapy 1975;21(suppl 1):27–35Google Scholar
34Lundberg, C, Gullers, K, Malmborg, AS. Antibiotics in sinus secretions. Lancet 1968;2:107–8Google Scholar
35Margaritis, VK, Ismailos, GS, Naxakis, SS, Mastronikolis, NS, Goumas, PD. Sinus fluid penetration of oral clarithromycin and azithromycin in patients with acute rhinosinusitis. Am J Rhinol 2007;21:574–8Google Scholar
36Pea, F, Marioni, G, Pavan, F, Staffieri, C, Bottin, R, Staffieri, A et al. Penetration of levofloxacin into paranasal sinuses mucosa of patients with chronic rhinosinusitis after a single 500 mg oral dose. Pharmacol Res 2007;55:38–41Google Scholar
37Stoeckel, K, Harell, M, Dan, M. Penetration of cefetamet pivoxil and cefuroxime axetil into the maxillary sinus mucosa at steady state. Antimicrob Agents Chemother 1996;40:780–3Google Scholar
38Tolsdorff, P. Penetration of ofloxacin into nasal tissues. Infection 1993;21:66–70Google Scholar
39Langdon, A, Crook, N, Dantas, G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med 2016;8:39Google Scholar
40Jakobsson, HE, Jernberg, C, Andersson, AF, Sjolund-Karlsson, M, Jansson, JK, Engstrand, L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 2010;5:e9836Google Scholar
41Zaura, E, Brandt, BW, Teixeira de Mattos, MJ, Buijs, MJ, Caspers, MP, Rashid, MU et al. Same exposure but two radically different responses to antibiotics: resilience of the salivary microbiome versus long-term microbial shifts in feces. MBio 2015;6:e01693–15Google Scholar
42Periti, P, Mazzei, T, Mini, E, Novelli, A. Clinical pharmacokinetic properties of the macrolide antibiotics. Effects of age and various pathophysiological states (Part I). Clin Pharmacokinet 1989;16:193–214Google Scholar
43Agwuh, KN, MacGowan, A. Pharmacokinetics and pharmacodynamics of the tetracyclines including glycylcyclines. J Antimicrob Chemother 2006;58:256–65Google Scholar
44Mouton, JW, Theuretzbacher, U, Craig, WA, Tulkens, PM, Derendorf, H, Cars, O. Tissue concentrations: do we ever learn? J Antimicrob Chemother 2008;61:235–7Google Scholar
45US Food and Drug Administration. Bioanalytical method validation guidance for industry. In: http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM070107.pdf [29 August 2018]Google Scholar
46Serralheiro, A, Alves, G, Falcao, AC. Bioanalysis of small-molecule drugs in nasal and paranasal tissues and secretions: current status and perspectives. Cent Eur J Chem 2012;10:686–702Google Scholar
47Bimazubute, MA, Rozet, E, Dizier, I, Gustin, P, Hubert, P, Crommen, J et al. Liquid chromatographic determination of enrofloxacin in nasal secretions and plasma of healthy pigs using restricted access material for on-line sample clean-up. J Chromatogr A 2007;1189:456–66Google Scholar
48Levine, JM, D'Antonio, CM. Elton revisited: a review of evidence linking diversity and invasibility. Oikos 1999;87:15–26Google Scholar
49Ramakrishnan, VR, Hauser, LH, Feazel, LM, Ir, D, Robertson, CE, Frank, DN. Sinus microbiota varies among chronic rhinosinusitis phenotypes and predicts surgical outcome. J Allergy Clin Immunol 2015;136:334–4210.1016/j.jaci.2015.02.008Google Scholar
50Turnbaugh, PJ, Ley, RE, Hamady, M. The human microbiome project. Nature 2007;449:804–1010.1038/nature06244Google Scholar
51Liu, CM, Soldanova, K, Nordstrom, L, Dwan, MG, Moss, OL, Contente-Cuomo, TL et al. Medical therapy reduces microbiota diversity and evenness in surgically recalcitrant chronic rhinosinusitis. Int Forum Allergy Rhinol 2013;3:775–8110.1002/alr.21195Google Scholar
52Liu, CM, Kohanski, MA, Mendiola, M. Impact of saline irrigation and topical corticosteroids on the postsurgical sinonasal microbiota. Int Forum Allergy Rhinol 2015;5:185–90Google Scholar
53Jain, R, Hoggard, M, Zoing, M, Jiang, Y, Biswas, K, Taylor, MW et al. The effect of medical treatments on the bacterial microbiome in patients with chronic rhinosinusitis: a pilot study. Int Forum Allergy Rhinol 2018;8:890–9Google Scholar
54Cleland, EJ, Bassiouni, A, Vreugde, S, Wormald, PJ. The bacterial microbiome in chronic rhinosinusitis: richness, diversity, postoperative changes, and patient outcomes. Am J Rhinol Allergy 2015;30:37–43Google Scholar
55Fokkens, WJ, Lund, VJ, Mullol, J, Bachert, C, Alobid, I, Baroody, F et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 2012;50:1–1210.4193/Rhino50E2Google Scholar
56Hauser, LJ, Ir, D, Kingdom, TT, Robertson, CE, Frank, DN, Ramakrishnan, VR. Investigation of bacterial repopulation after sinus surgery and perioperative antibiotics. Int Forum Allergy Rhinol 2015;6:34–40Google Scholar
57Shehab, N, Patel, PR, Srinivasan, A, Budnitz, DS. Emergency department visits for antibiotic-associated adverse events. Clin Infect Dis 2008;47:735–43Google Scholar
58Kiguba, R, Karamagi, C, Bird, S. Antibiotic-associated suspected adverse drug reactions among hospitalized patients in Uganda: a prospective cohort study. Pharmacol Res Perspect 2017;5:e00298Google Scholar
59Korpela, K, Salonen, A, Virta, LJ, Kekkonen, RA, Forslund, K, Bork, P et al. Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children. Nat Commun 2016;7:10410Google Scholar
60Raymond, F, Deraspe, M, Boissinot, M, Bergeron, MG, Corbeil, J. Partial recovery of microbiomes after antibiotic treatment. Gut Microbes 2016;7:428–34Google Scholar
61Angelakis, E, Million, M, Kankoe, S, Lagier, JC, Armougom, F, Giorgi, R et al. Abnormal weight gain and gut microbiota modifications are side effects of long-term doxycycline and hydroxychloroquine treatment. Antimicrob Agents Chemother 2014;58:3342–7Google Scholar
62Becattini, S, Taur, Y, Pamer, EG. Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol Med 2016;22:458–78Google Scholar
63Ianiro, G, Tilg, H, Gasbarrini, A. Antibiotics as deep modulators of gut microbiota: between good and evil. Gut 2016;65:1906–15Google Scholar
64Mikkelsen, KH, Frost, M, Bahl, MI, Licht, TR, Jensen, US, Rosenburg, J et al. Effect of antibiotics on gut microbiota, gut hormones and glucose metabolism. PLoS One 2015;10:e0142352Google Scholar
65Yoon, MY, Yoon, SS. Disruption of the gut ecosystem by antibiotics. Yonsei Med J 2018;59:4–12Google Scholar
66Gevers, D, Kugathasan, S, Denson, LA, Vázquez-Baeza, Y, Van Treuren, W, Ren, B et al. The treatment-naïve microbiome in new-onset Crohn's disease. Cell Host Microbe 2014;15:382–92Google Scholar
67Slimings, C, Riley, TV. Antibiotics and hospital-acquired Clostridium difficile infection: update of systematic review and meta-analysis. J Antimicrob Chemother 2014;69:881–91Google Scholar
68Boursi, B, Mamtani, R, Haynes, K, Yang, YX. The effect of past antibiotic exposure on diabetes risk. Eur J Endocrinol 2015;172:639–48Google Scholar
69Villarreal, AA, Aberger, FJ, Benrud, R, Gundrum, JD. Use of broad-spectrum antibiotics and the development of irritable bowel syndrome. WMJ 2012;111:17–20Google Scholar
70Lankelma, JM, Cranendonk, DR, Belzer, C, de Vos, AF, de Vos, WM, van der Poll, T et al. Antibiotic-induced gut microbiota disruption during human endotoxemia: a randomised controlled study. Gut 2017;66:1623–30Google Scholar