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Erschienen in: European Journal of Clinical Microbiology & Infectious Diseases 6/2018

20.03.2018 | Original Article

Intrapulmonary percussive ventilation improves lung function in cystic fibrosis patients chronically colonized with Pseudomonas aeruginosa: a pilot cross-over study

verfasst von: Jozef Dingemans, Hanneke Eyns, Julie Willekens, Pieter Monsieurs, Rob Van Houdt, Pierre Cornelis, Anne Malfroot, Aurélie Crabbé

Erschienen in: European Journal of Clinical Microbiology & Infectious Diseases | Ausgabe 6/2018

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Abstract

High levels of shear stress can prevent and disrupt Pseudomonas aeruginosa biofilm formation in vitro. Intrapulmonary percussive ventilation (IPV) could be used to introduce shear stress into the lungs of cystic fibrosis (CF) patients to disrupt biofilms in vivo. We performed a first-of-its-kind pilot clinical study to evaluate short-term IPV therapy at medium (200 bursts per minute, bpm) and high frequency (400 bpm) as compared to autogenic drainage (AD) on lung function and the behavior of P. aeruginosa in the CF lung in four patients who are chronically colonized by P. aeruginosa. A significant difference between the three treatment groups was observed for both the forced expiratory volume in 1 s (FEV1) and the forced vital capacity (FVC) (p < 0.05). More specifically, IPV at high frequency significantly increased FEV1 and FVC compared to AD (p < 0.05) and IPV at medium frequency (p < 0.001). IPV at high frequency enhanced the expression levels of P. aeruginosa planktonic marker genes, which was less pronounced with IPV at medium frequency or AD. In conclusion, IPV at high frequency could potentially alter the behavior of P. aeruginosa in the CF lung and improve lung function. Trial registration: The trail was retrospectively registered at the ISRCTN registry on 6 June 2013, under trial registration number ISRCTN75391385.
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Literatur
1.
Zurück zum Zitat Harrison F (2007) Microbial ecology of the cystic fibrosis lung. Microbiology 153(Pt 4):917–923CrossRefPubMed Harrison F (2007) Microbial ecology of the cystic fibrosis lung. Microbiology 153(Pt 4):917–923CrossRefPubMed
2.
Zurück zum Zitat Hauser AR, Jain M, Bar-Meir M, McColley SA (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24(1):29–70CrossRefPubMedPubMedCentral Hauser AR, Jain M, Bar-Meir M, McColley SA (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24(1):29–70CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Ahlgren HG, Benedetti A, Landry JS, Bernier J, Matouk E, Radzioch D, Lands LC, Rousseau S, Nguyen D (2015) Clinical outcomes associated with Staphylococcus aureus and Pseudomonas aeruginosa airway infections in adult cystic fibrosis patients. BMC Pulm Med 15:67CrossRefPubMedPubMedCentral Ahlgren HG, Benedetti A, Landry JS, Bernier J, Matouk E, Radzioch D, Lands LC, Rousseau S, Nguyen D (2015) Clinical outcomes associated with Staphylococcus aureus and Pseudomonas aeruginosa airway infections in adult cystic fibrosis patients. BMC Pulm Med 15:67CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, Hoiby N, Molin S (2012) Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10(12):841–851CrossRefPubMed Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, Hoiby N, Molin S (2012) Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10(12):841–851CrossRefPubMed
5.
Zurück zum Zitat Marvig RL, Sommer LM, Molin S, Johansen HK (2015) Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat Genet 47(1):57–64CrossRefPubMed Marvig RL, Sommer LM, Molin S, Johansen HK (2015) Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat Genet 47(1):57–64CrossRefPubMed
6.
Zurück zum Zitat Hogardt M, Heesemann J (2010) Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int J Med Microbiol 300(8):557–562CrossRefPubMed Hogardt M, Heesemann J (2010) Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int J Med Microbiol 300(8):557–562CrossRefPubMed
7.
Zurück zum Zitat Jensen ET, Kharazmi A, Lam K, Costerton JW, Hoiby N (1990) Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 58(7):2383–2385PubMedPubMedCentral Jensen ET, Kharazmi A, Lam K, Costerton JW, Hoiby N (1990) Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 58(7):2383–2385PubMedPubMedCentral
8.
Zurück zum Zitat Anwar H, Strap JL, Costerton JW (1992) Susceptibility of biofilm cells of Pseudomonas aeruginosa to bactericidal actions of whole blood and serum. FEMS Microbiol Lett 71(3):235–241CrossRefPubMed Anwar H, Strap JL, Costerton JW (1992) Susceptibility of biofilm cells of Pseudomonas aeruginosa to bactericidal actions of whole blood and serum. FEMS Microbiol Lett 71(3):235–241CrossRefPubMed
9.
Zurück zum Zitat Taylor PK, Yeung AT, Hancock RE (2014) Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol 191:121–130CrossRefPubMed Taylor PK, Yeung AT, Hancock RE (2014) Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol 191:121–130CrossRefPubMed
10.
Zurück zum Zitat Crabbé A, De Boever P, Van Houdt R, Moors H, Mergeay M, Cornelis P (2008) Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PA01. Environ Microbiol 10(8):2098–2110CrossRefPubMed Crabbé A, De Boever P, Van Houdt R, Moors H, Mergeay M, Cornelis P (2008) Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PA01. Environ Microbiol 10(8):2098–2110CrossRefPubMed
11.
Zurück zum Zitat Crabbé A, Pycke B, Van Houdt R, Monsieurs P, Nickerson C, Leys N, Cornelis P (2010) Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation. Environ Microbiol 12(6):1545–1564PubMed Crabbé A, Pycke B, Van Houdt R, Monsieurs P, Nickerson C, Leys N, Cornelis P (2010) Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation. Environ Microbiol 12(6):1545–1564PubMed
13.
Zurück zum Zitat Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47(1):317–323CrossRefPubMedPubMedCentral Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47(1):317–323CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Alhede M, Kragh KN, Qvortrup K, Allesen-Holm M, van Gennip M, Christensen LD, Jensen PO, Nielsen AK, Parsek M, Wozniak D, Molin S, Tolker-Nielsen T, Hoiby N, Givskov M, Bjarnsholt T (2011) Phenotypes of non-attached Pseudomonas aeruginosa aggregates resemble surface attached biofilm. PLoS One 6(11):e27943CrossRefPubMedPubMedCentral Alhede M, Kragh KN, Qvortrup K, Allesen-Holm M, van Gennip M, Christensen LD, Jensen PO, Nielsen AK, Parsek M, Wozniak D, Molin S, Tolker-Nielsen T, Hoiby N, Givskov M, Bjarnsholt T (2011) Phenotypes of non-attached Pseudomonas aeruginosa aggregates resemble surface attached biofilm. PLoS One 6(11):e27943CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Lucangelo U, Fontanesi L, Antonaglia V, Pellis T, Berlot G, Liguori G, Bird FM, Gullo A (2003) High frequency percussive ventilation (HFPV). Principles and technique. Minerva Anestesiol 69(11):841–848 848-851PubMed Lucangelo U, Fontanesi L, Antonaglia V, Pellis T, Berlot G, Liguori G, Bird FM, Gullo A (2003) High frequency percussive ventilation (HFPV). Principles and technique. Minerva Anestesiol 69(11):841–848 848-851PubMed
16.
Zurück zum Zitat Varekojis SM, Douce FH, Flucke RL, Filbrun DA, Tice JS, McCoy KS, Castile RG (2003) A comparison of the therapeutic effectiveness of and preference for postural drainage and percussion, intrapulmonary percussive ventilation, and high-frequency chest wall compression in hospitalized cystic fibrosis patients. Respir Care 48(1):24–28PubMed Varekojis SM, Douce FH, Flucke RL, Filbrun DA, Tice JS, McCoy KS, Castile RG (2003) A comparison of the therapeutic effectiveness of and preference for postural drainage and percussion, intrapulmonary percussive ventilation, and high-frequency chest wall compression in hospitalized cystic fibrosis patients. Respir Care 48(1):24–28PubMed
17.
Zurück zum Zitat Chevaillier J (1984) Autogenic drainage. In: Lawson D (ed) Cystic fibrosis horizons. John Wiley, Chichester, p 235 Chevaillier J (1984) Autogenic drainage. In: Lawson D (ed) Cystic fibrosis horizons. John Wiley, Chichester, p 235
18.
Zurück zum Zitat Schoni MH (1989) Autogenic drainage: a modern approach to physiotherapy in cystic fibrosis. J R Soc Med 82(Suppl 16):32–37PubMedPubMedCentral Schoni MH (1989) Autogenic drainage: a modern approach to physiotherapy in cystic fibrosis. J R Soc Med 82(Suppl 16):32–37PubMedPubMedCentral
19.
Zurück zum Zitat Agostini P, Knowles N (2007) Autogenic drainage: the technique, physiological basis and evidence. Physiotherapy 93:157–163CrossRef Agostini P, Knowles N (2007) Autogenic drainage: the technique, physiological basis and evidence. Physiotherapy 93:157–163CrossRef
20.
Zurück zum Zitat Van Ginderdeuren F, Verbanck S, Van Cauwelaert K, Vanlaethem S, Schuermans D, Vincken W, Malfroot A (2008) Chest physiotherapy in cystic fibrosis: short-term effects of autogenic drainage preceded by wet inhalation of saline versus autogenic drainage preceded by intrapulmonary percussive ventilation with saline. Respiration 76(2):175–180CrossRefPubMed Van Ginderdeuren F, Verbanck S, Van Cauwelaert K, Vanlaethem S, Schuermans D, Vincken W, Malfroot A (2008) Chest physiotherapy in cystic fibrosis: short-term effects of autogenic drainage preceded by wet inhalation of saline versus autogenic drainage preceded by intrapulmonary percussive ventilation with saline. Respiration 76(2):175–180CrossRefPubMed
21.
Zurück zum Zitat Pirnay JP, Bilocq F, Pot B, Cornelis P, Zizi M, Van Eldere J, Deschaght P, Vaneechoutte M, Jennes S, Pitt T, De Vos D (2009) Pseudomonas aeruginosa population structure revisited. PLoS One 4(11):e7740CrossRefPubMedPubMedCentral Pirnay JP, Bilocq F, Pot B, Cornelis P, Zizi M, Van Eldere J, Deschaght P, Vaneechoutte M, Jennes S, Pitt T, De Vos D (2009) Pseudomonas aeruginosa population structure revisited. PLoS One 4(11):e7740CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Dingemans J, Ye L, Hildebrand F, Tontodonati F, Craggs M, Bilocq F, De Vos D, Crabbé A, Van Houdt R, Malfroot A, Cornelis P (2014) The deletion of TonB-dependent receptor genes is part of the genome reduction process that occurs during adaptation of Pseudomonas aeruginosa to the cystic fibrosis lung. Pathog Dis 71(1):26–38CrossRefPubMed Dingemans J, Ye L, Hildebrand F, Tontodonati F, Craggs M, Bilocq F, De Vos D, Crabbé A, Van Houdt R, Malfroot A, Cornelis P (2014) The deletion of TonB-dependent receptor genes is part of the genome reduction process that occurs during adaptation of Pseudomonas aeruginosa to the cystic fibrosis lung. Pathog Dis 71(1):26–38CrossRefPubMed
23.
Zurück zum Zitat Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470CrossRefPubMedPubMedCentral Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Son MS, Matthews WJ Jr, Kang Y, Nguyen DT, Hoang TT (2007) In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun 75(11):5313–5324CrossRefPubMedPubMedCentral Son MS, Matthews WJ Jr, Kang Y, Nguyen DT, Hoang TT (2007) In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun 75(11):5313–5324CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMed Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMed
26.
Zurück zum Zitat Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed
27.
Zurück zum Zitat Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48CrossRef Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48CrossRef
28.
Zurück zum Zitat Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363CrossRefPubMed Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363CrossRefPubMed
29.
Zurück zum Zitat Maeda Y, Elborn JS, Parkins MD, Reihill J, Goldsmith CE, Coulter WA, Mason C, Millar BC, Dooley JS, Lowery CJ, Ennis M, Rendall JC, Moore JE (2011) Population structure and characterization of viridans group streptococci (VGS) including Streptococcus pneumoniae isolated from adult patients with cystic fibrosis (CF). J Cyst Fibros 10(2):133–139CrossRefPubMed Maeda Y, Elborn JS, Parkins MD, Reihill J, Goldsmith CE, Coulter WA, Mason C, Millar BC, Dooley JS, Lowery CJ, Ennis M, Rendall JC, Moore JE (2011) Population structure and characterization of viridans group streptococci (VGS) including Streptococcus pneumoniae isolated from adult patients with cystic fibrosis (CF). J Cyst Fibros 10(2):133–139CrossRefPubMed
30.
Zurück zum Zitat Lim YW, Haynes M, Furlan M, Robertson CE, Harris JK, Rohwer F (2014) Purifying the impure: sequencing metagenomes and metatranscriptomes from complex animal-associated samples. J Vis Exp 94 Lim YW, Haynes M, Furlan M, Robertson CE, Harris JK, Rohwer F (2014) Purifying the impure: sequencing metagenomes and metatranscriptomes from complex animal-associated samples. J Vis Exp 94
31.
Zurück zum Zitat Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, Hancock RE, Brinkman FS (2011) Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39(Database issue):D596–D600CrossRefPubMed Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, Hancock RE, Brinkman FS (2011) Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39(Database issue):D596–D600CrossRefPubMed
32.
Zurück zum Zitat Hunter RC, Asfour F, Dingemans J, Osuna BL, Samad T, Malfroot A, Cornelis P, Newman DK (2013) Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. MBio 4(4) Hunter RC, Asfour F, Dingemans J, Osuna BL, Samad T, Malfroot A, Cornelis P, Newman DK (2013) Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. MBio 4(4)
33.
Zurück zum Zitat Gifford AH, Willger SD, Dolben EL, Moulton LA, Dorman DB, Bean H, Hill JE, Hampton TH, Ashare A, Hogan DA (2016) Use of a multiplex transcript method for analysis of Pseudomonas aeruginosa gene expression profiles in the cystic fibrosis lung. Infect Immun 84(10):2995–3006CrossRefPubMedPubMedCentral Gifford AH, Willger SD, Dolben EL, Moulton LA, Dorman DB, Bean H, Hill JE, Hampton TH, Ashare A, Hogan DA (2016) Use of a multiplex transcript method for analysis of Pseudomonas aeruginosa gene expression profiles in the cystic fibrosis lung. Infect Immun 84(10):2995–3006CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Cigana C, Melotti P, Baldan R, Pedretti E, Pintani E, Iansa P, De Fino I, Favari F, Bergamini G, Tridello G, Cirillo DM, Assael BM, Bragonzi A (2016) Genotypic and phenotypic relatedness of Pseudomonas aeruginosa isolates among the major cystic fibrosis patient cohort in Italy. BMC Microbiol 16(1):142CrossRefPubMedPubMedCentral Cigana C, Melotti P, Baldan R, Pedretti E, Pintani E, Iansa P, De Fino I, Favari F, Bergamini G, Tridello G, Cirillo DM, Assael BM, Bragonzi A (2016) Genotypic and phenotypic relatedness of Pseudomonas aeruginosa isolates among the major cystic fibrosis patient cohort in Italy. BMC Microbiol 16(1):142CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Workentine ML, Sibley CD, Glezerson B, Purighalla S, Norgaard-Gron JC, Parkins MD, Rabin HR, Surette MG (2013) Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS One 8(4):e60225CrossRefPubMedPubMedCentral Workentine ML, Sibley CD, Glezerson B, Purighalla S, Norgaard-Gron JC, Parkins MD, Rabin HR, Surette MG (2013) Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS One 8(4):e60225CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Balasubramanian D, Schneper L, Kumari H, Mathee K (2013) A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41(1):1–20CrossRefPubMed Balasubramanian D, Schneper L, Kumari H, Mathee K (2013) A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41(1):1–20CrossRefPubMed
38.
Zurück zum Zitat Wilkins M, Hall-Stoodley L, Allan RN, Faust SN (2014) New approaches to the treatment of biofilm-related infections. J Inf Secur 69(Suppl 1):S47–S52 Wilkins M, Hall-Stoodley L, Allan RN, Faust SN (2014) New approaches to the treatment of biofilm-related infections. J Inf Secur 69(Suppl 1):S47–S52
39.
Zurück zum Zitat Li XH, Lee JH (2017) Antibiofilm agents: a new perspective for antimicrobial strategy. J Microbiol 55(10):753–766CrossRefPubMed Li XH, Lee JH (2017) Antibiofilm agents: a new perspective for antimicrobial strategy. J Microbiol 55(10):753–766CrossRefPubMed
40.
Zurück zum Zitat Algburi A, Comito N, Kashtanov D, Dicks LM, Chikindas ML (2017) Control of biofilm formation: antibiotics and beyond. Appl Environ Microbiol 83(3) Algburi A, Comito N, Kashtanov D, Dicks LM, Chikindas ML (2017) Control of biofilm formation: antibiotics and beyond. Appl Environ Microbiol 83(3)
41.
Zurück zum Zitat Natale JE, Pfeifle J, Homnick DN (1994) Comparison of intrapulmonary percussive ventilation and chest physiotherapy: a pilot study in patients with cystic fibrosis. Chest 105(6):1789–1793CrossRefPubMed Natale JE, Pfeifle J, Homnick DN (1994) Comparison of intrapulmonary percussive ventilation and chest physiotherapy: a pilot study in patients with cystic fibrosis. Chest 105(6):1789–1793CrossRefPubMed
42.
Zurück zum Zitat Homnick DN, White F, de Castro C (1995) Comparison of effects of an intrapulmonary percussive ventilator to standard aerosol and chest physiotherapy in treatment of cystic fibrosis. Pediatr Pulmonol 20(1):50–55CrossRefPubMed Homnick DN, White F, de Castro C (1995) Comparison of effects of an intrapulmonary percussive ventilator to standard aerosol and chest physiotherapy in treatment of cystic fibrosis. Pediatr Pulmonol 20(1):50–55CrossRefPubMed
43.
Zurück zum Zitat Barthe C, Nandakumar S, Derlich L, Macey J, Bui S, Fayon M, Crouzet M, Garbay B, Vilain S, Costaglioli P (2015) Exploring the expression of Pseudomonas aeruginosa genes directly from sputa of cystic fibrosis patients. Lett Appl Microbiol 61(5):423–8. https://doi.org/10.1111/lam.12465 Barthe C, Nandakumar S, Derlich L, Macey J, Bui S, Fayon M, Crouzet M, Garbay B, Vilain S, Costaglioli P (2015) Exploring the expression of Pseudomonas aeruginosa genes directly from sputa of cystic fibrosis patients. Lett Appl Microbiol 61(5):423–8. https://​doi.​org/​10.​1111/​lam.​12465
44.
Zurück zum Zitat Davies EV, James CE, Brockhurst MA, Winstanley C (2017) Evolutionary diversification of Pseudomonas aeruginosa in an artificial sputum model. BMC Microbiol 17(1):3CrossRefPubMedPubMedCentral Davies EV, James CE, Brockhurst MA, Winstanley C (2017) Evolutionary diversification of Pseudomonas aeruginosa in an artificial sputum model. BMC Microbiol 17(1):3CrossRefPubMedPubMedCentral
Metadaten
Titel
Intrapulmonary percussive ventilation improves lung function in cystic fibrosis patients chronically colonized with Pseudomonas aeruginosa: a pilot cross-over study
verfasst von
Jozef Dingemans
Hanneke Eyns
Julie Willekens
Pieter Monsieurs
Rob Van Houdt
Pierre Cornelis
Anne Malfroot
Aurélie Crabbé
Publikationsdatum
20.03.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Clinical Microbiology & Infectious Diseases / Ausgabe 6/2018
Print ISSN: 0934-9723
Elektronische ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-018-3232-8

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