Skip to main content
Top
Published in: Antimicrobial Resistance & Infection Control 1/2020

Open Access 01-12-2020 | Expectoration | Short report

Comparative evaluation of the effect of different growth media on in vitro sensitivity to azithromycin in multi-drug resistant Pseudomonas aeruginosa isolated from cystic fibrosis patients

Authors: Michael Sörensen, Bakhodur Khakimov, Dennis Nurjadi, Sébastien Boutin, Buqing Yi, Alexander H. Dalpke, Tatjana Eigenbrod

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2020

Login to get access

Abstract

Long-term treatment with azithromycin is a therapeutic option in Cystic Fibrosis (CF) patients chronically infected with P. aeruginosa. It was recently shown that azithromycin has direct antimicrobial activity when P. aeruginosa isolates are tested in Roswell Park Memorial Institute medium supplemented with fetal calf serum (RPMI 1640/FCS) by broth microdilution. We now investigated whether (i) azithromycin might also be active against multidrug resistant (MDR) P. aeruginosa isolated from CF patients and (ii) how in vitro sensitivity assays perform in synthetic cystic fibrosis sputum medium (SCFM), a medium that mimics the particular CF airway environment. In 17 (59%) out of 29 MDR P. aeruginosa CF isolates MICs for azithromycin ranged between 0.25 and 8 μg/ml and 12 isolates (41%) showed a MIC ≥512 μg/ml when measured in RPMI/FCS. In contrast, MICs were ≥ 256 μg/ml for all P. aeruginosa MDR isolates when tested in either SCFM or in conventional cation-adjusted Mueller Hinton Broth. High MIC values observed in CF adapted medium SCFM for both PAO1 and MDR P. aeruginosa CF isolates, as opposed to findings in RPMI, argue against routine azithromycin MIC testing of CF isolates.
Literature
1.
go back to reference Mall MA, Hartl D. CFTR: cystic fibrosis and beyond. Eur Respir J. 2014;44(4):1042–54.CrossRef Mall MA, Hartl D. CFTR: cystic fibrosis and beyond. Eur Respir J. 2014;44(4):1042–54.CrossRef
2.
go back to reference Lund-Palau H, Turnbull AR, Bush A, Bardin E, Cameron L, Soren O, et al. Pseudomonas aeruginosa infection in cystic fibrosis: pathophysiological mechanisms and therapeutic approaches. Expert Rev Respir Med. 2016;10(6):685–97.CrossRef Lund-Palau H, Turnbull AR, Bush A, Bardin E, Cameron L, Soren O, et al. Pseudomonas aeruginosa infection in cystic fibrosis: pathophysiological mechanisms and therapeutic approaches. Expert Rev Respir Med. 2016;10(6):685–97.CrossRef
3.
go back to reference Mayer-Hamblett N, Kloster M, Rosenfeld M, Gibson RL, Retsch-Bogart GZ, Emerson J, et al. Impact of sustained eradication of new Pseudomonas aeruginosa infection on long-term outcomes in cystic fibrosis. Clin Infect Dis. 2015;61(5):707–15.CrossRef Mayer-Hamblett N, Kloster M, Rosenfeld M, Gibson RL, Retsch-Bogart GZ, Emerson J, et al. Impact of sustained eradication of new Pseudomonas aeruginosa infection on long-term outcomes in cystic fibrosis. Clin Infect Dis. 2015;61(5):707–15.CrossRef
5.
go back to reference Stefani S, Campana S, Cariani L, Carnovale V, Colombo C, Lleo MM, et al. Relevance of multidrug-resistant Pseudomonas aeruginosa infections in cystic fibrosis. Int J Med Microbiol. 2017;307(6):353–62.CrossRef Stefani S, Campana S, Cariani L, Carnovale V, Colombo C, Lleo MM, et al. Relevance of multidrug-resistant Pseudomonas aeruginosa infections in cystic fibrosis. Int J Med Microbiol. 2017;307(6):353–62.CrossRef
7.
go back to reference Mogayzel PJ Jr, Naureckas ET, Robinson KA, Mueller G, Hadjiliadis D, Hoag JB, et al. Cystic fibrosis pulmonary guidelines. Chronic medications for maintenance of lung health. Am J Respir Crit Care Med. 2013;187(7):680–9.CrossRef Mogayzel PJ Jr, Naureckas ET, Robinson KA, Mueller G, Hadjiliadis D, Hoag JB, et al. Cystic fibrosis pulmonary guidelines. Chronic medications for maintenance of lung health. Am J Respir Crit Care Med. 2013;187(7):680–9.CrossRef
8.
go back to reference Principi N, Blasi F, Esposito S. Azithromycin use in patients with cystic fibrosis. Eur J Clin Microbiol Infect Dis. 2015;34(6):1071–9.CrossRef Principi N, Blasi F, Esposito S. Azithromycin use in patients with cystic fibrosis. Eur J Clin Microbiol Infect Dis. 2015;34(6):1071–9.CrossRef
9.
go back to reference Saiman L, Marshall BC, Mayer-Hamblett N, Burns JL, Quittner AL, Cibene DA, et al. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA. 2003;290(13):1749–56.CrossRef Saiman L, Marshall BC, Mayer-Hamblett N, Burns JL, Quittner AL, Cibene DA, et al. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA. 2003;290(13):1749–56.CrossRef
10.
go back to reference Imperi F, Leoni L, Visca P. Antivirulence activity of azithromycin in Pseudomonas aeruginosa. Front Microbiol. 2014;5:178.CrossRef Imperi F, Leoni L, Visca P. Antivirulence activity of azithromycin in Pseudomonas aeruginosa. Front Microbiol. 2014;5:178.CrossRef
11.
go back to reference Buyck JM, Plesiat P, Traore H, Vanderbist F, Tulkens PM, Van Bambeke F. Increased susceptibility of Pseudomonas aeruginosa to macrolides and ketolides in eukaryotic cell culture media and biological fluids due to decreased expression of oprM and increased outer-membrane permeability. Clin Infect Dis. 2012;55(4):534–42.CrossRef Buyck JM, Plesiat P, Traore H, Vanderbist F, Tulkens PM, Van Bambeke F. Increased susceptibility of Pseudomonas aeruginosa to macrolides and ketolides in eukaryotic cell culture media and biological fluids due to decreased expression of oprM and increased outer-membrane permeability. Clin Infect Dis. 2012;55(4):534–42.CrossRef
13.
go back to reference Palmer KL, Aye LM, Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol. 2007;189(22):8079–87.CrossRef Palmer KL, Aye LM, Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol. 2007;189(22):8079–87.CrossRef
14.
go back to reference Hogardt MH, Susanne; Balke, Beate; Kahl, Barbara C.; Schmoldt, Sabine; Leitritz, Lorenz; Jäger, Gundula; Kappler, Matthias; Suerbaum, Sebastian; Heesemann, Jürgen Atemwegsinfektionen bei Mukoviszidose. Qualitätsstandards in der mikrobiologisch-infektiologischen Diagnostik 2006;MiQ24. Hogardt MH, Susanne; Balke, Beate; Kahl, Barbara C.; Schmoldt, Sabine; Leitritz, Lorenz; Jäger, Gundula; Kappler, Matthias; Suerbaum, Sebastian; Heesemann, Jürgen Atemwegsinfektionen bei Mukoviszidose. Qualitätsstandards in der mikrobiologisch-infektiologischen Diagnostik 2006;MiQ24.
15.
go back to reference Matuschek E, Ahman J, Webster C, Kahlmeter G. Antimicrobial susceptibility testing of colistin - evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin Microbiol Infect. 2018;24(8):865–70.CrossRef Matuschek E, Ahman J, Webster C, Kahlmeter G. Antimicrobial susceptibility testing of colistin - evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin Microbiol Infect. 2018;24(8):865–70.CrossRef
16.
go back to reference Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal. 2016;6(2):71–9.CrossRef Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal. 2016;6(2):71–9.CrossRef
17.
go back to reference Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 2008;3(2):163–75.CrossRef Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 2008;3(2):163–75.CrossRef
18.
go back to reference Oberhardt MA, Puchalka J, Fryer KE, Martins dos Santos VA, Papin JA. Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1. J Bacteriol. 2008;190(8):2790–803.CrossRef Oberhardt MA, Puchalka J, Fryer KE, Martins dos Santos VA, Papin JA. Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1. J Bacteriol. 2008;190(8):2790–803.CrossRef
19.
go back to reference Pressler T, Bohmova C, Conway S, Dumcius S, Hjelte L, Hoiby N, et al. Chronic Pseudomonas aeruginosa infection definition: EuroCareCF working group report. J Cyst Fibros. 2011;10(Suppl 2):S75–8.CrossRef Pressler T, Bohmova C, Conway S, Dumcius S, Hjelte L, Hoiby N, et al. Chronic Pseudomonas aeruginosa infection definition: EuroCareCF working group report. J Cyst Fibros. 2011;10(Suppl 2):S75–8.CrossRef
20.
go back to reference Marvig RL, Sondergaard MS, Damkiaer S, Hoiby N, Johansen HK, Molin S, et al. Mutations in 23S rRNA confer resistance against azithromycin in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2012;56(8):4519–21.CrossRef Marvig RL, Sondergaard MS, Damkiaer S, Hoiby N, Johansen HK, Molin S, et al. Mutations in 23S rRNA confer resistance against azithromycin in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2012;56(8):4519–21.CrossRef
21.
go back to reference Castellani C, Duff AJA, Bell SC, Heijerman HGM, Munck A, Ratjen F, et al. ECFS best practice guidelines: the 2018 revision. J Cyst Fibros. 2018;17(2):153–78.CrossRef Castellani C, Duff AJA, Bell SC, Heijerman HGM, Munck A, Ratjen F, et al. ECFS best practice guidelines: the 2018 revision. J Cyst Fibros. 2018;17(2):153–78.CrossRef
22.
go back to reference Molinari G, Guzman CA, Pesce A, Schito GC. Inhibition of Pseudomonas aeruginosa virulence factors by subinhibitory concentrations of azithromycin and other macrolide antibiotics. J Antimicrob Chemother. 1993;31(5):681–8.CrossRef Molinari G, Guzman CA, Pesce A, Schito GC. Inhibition of Pseudomonas aeruginosa virulence factors by subinhibitory concentrations of azithromycin and other macrolide antibiotics. J Antimicrob Chemother. 1993;31(5):681–8.CrossRef
23.
go back to reference Diaz Iglesias Y, Wilms T, Vanbever R, Van Bambeke F. Activity of antibiotics against Staphylococcus aureus in an in vitro model of biofilms in the context of cystic fibrosis: influence of the culture medium. Antimicrob Agents Chemother. 2019;63(7):e00602–19.CrossRef Diaz Iglesias Y, Wilms T, Vanbever R, Van Bambeke F. Activity of antibiotics against Staphylococcus aureus in an in vitro model of biofilms in the context of cystic fibrosis: influence of the culture medium. Antimicrob Agents Chemother. 2019;63(7):e00602–19.CrossRef
24.
go back to reference Swatton JE, Davenport PW, Maunders EA, Griffin JL, Lilley KS, Welch M. Impact of azithromycin on the quorum sensing-controlled proteome of Pseudomonas aeruginosa. PLoS One. 2016;11(1):e0147698.CrossRef Swatton JE, Davenport PW, Maunders EA, Griffin JL, Lilley KS, Welch M. Impact of azithromycin on the quorum sensing-controlled proteome of Pseudomonas aeruginosa. PLoS One. 2016;11(1):e0147698.CrossRef
25.
go back to reference Godeke J, Pustelny C, Haussler S. Recycling of peptidyl-tRNAs by peptidyl-tRNA hydrolase counteracts azithromycin-mediated effects on Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2013;57(4):1617–24.CrossRef Godeke J, Pustelny C, Haussler S. Recycling of peptidyl-tRNAs by peptidyl-tRNA hydrolase counteracts azithromycin-mediated effects on Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2013;57(4):1617–24.CrossRef
26.
go back to reference Scoffone VC, Trespidi G, Chiarelli LR, Barbieri G, Buroni S. Quorum sensing as antivirulence target in cystic fibrosis pathogens. Int J Mol Sci. 2019;20:1838.CrossRef Scoffone VC, Trespidi G, Chiarelli LR, Barbieri G, Buroni S. Quorum sensing as antivirulence target in cystic fibrosis pathogens. Int J Mol Sci. 2019;20:1838.CrossRef
27.
go back to reference Kariminik A, Baseri-Salehi M, Kheirkhah B. Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol Lett. 2017;190:1–6.CrossRef Kariminik A, Baseri-Salehi M, Kheirkhah B. Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol Lett. 2017;190:1–6.CrossRef
28.
go back to reference Saiman L, Anstead M, Mayer-Hamblett N, Lands LC, Kloster M, Hocevar-Trnka J, et al. Effect of azithromycin on pulmonary function in patients with cystic fibrosis uninfected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA. 2010;303(17):1707–15.CrossRef Saiman L, Anstead M, Mayer-Hamblett N, Lands LC, Kloster M, Hocevar-Trnka J, et al. Effect of azithromycin on pulmonary function in patients with cystic fibrosis uninfected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA. 2010;303(17):1707–15.CrossRef
Metadata
Title
Comparative evaluation of the effect of different growth media on in vitro sensitivity to azithromycin in multi-drug resistant Pseudomonas aeruginosa isolated from cystic fibrosis patients
Authors
Michael Sörensen
Bakhodur Khakimov
Dennis Nurjadi
Sébastien Boutin
Buqing Yi
Alexander H. Dalpke
Tatjana Eigenbrod
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2020
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-020-00859-7

Other articles of this Issue 1/2020

Antimicrobial Resistance & Infection Control 1/2020 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine