Pseudomonas aeruginosa in Bronchiectasis

Laia Fernández-Barat; Victoria Alcaraz-Serrano; Rosanel Amaro; Antoni Torres

doi:10.1055/s-0041-1730921

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2021; 42(04): 587-594
DOI: 10.1055/s-0041-1730921

Review Article

Pseudomonas aeruginosa in Bronchiectasis

Authors

Laia Fernández-Barat

¹Cellex Laboratory, CibeRes (Centro de Investigación Biomédica en Red de Enfermedades Respiratorias, 06/06/0028), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain

²School of Medicine, University of Barcelona, Barcelona, Spain

³Department of Pneumology, Respiratory Institute, Hospital Clinic of Barcelona, Spain
Victoria Alcaraz-Serrano

¹Cellex Laboratory, CibeRes (Centro de Investigación Biomédica en Red de Enfermedades Respiratorias, 06/06/0028), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain

²School of Medicine, University of Barcelona, Barcelona, Spain

³Department of Pneumology, Respiratory Institute, Hospital Clinic of Barcelona, Spain
Rosanel Amaro

¹Cellex Laboratory, CibeRes (Centro de Investigación Biomédica en Red de Enfermedades Respiratorias, 06/06/0028), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain

²School of Medicine, University of Barcelona, Barcelona, Spain

³Department of Pneumology, Respiratory Institute, Hospital Clinic of Barcelona, Spain
Antoni Torres

¹Cellex Laboratory, CibeRes (Centro de Investigación Biomédica en Red de Enfermedades Respiratorias, 06/06/0028), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain

²School of Medicine, University of Barcelona, Barcelona, Spain

³Department of Pneumology, Respiratory Institute, Hospital Clinic of Barcelona, Spain

Abstract

Pseudomonas aeruginosa (PA) in patients with bronchiectasis (BE) is associated with a poor outcome and quality of life, and its presence is considered a marker of disease severity. This opportunistic pathogen is known for its ability to produce biofilms on biotic or abiotic surfaces and to survive environmental stress exerted by antimicrobials, inflammation, and nutrient or oxygen depletion. The presence of PA biofilms has been linked to chronic respiratory infection in cystic fibrosis but not in BE. There is considerable inconsistency in the reported infection/eradication rates of PA and chronic PA. In addition, inadequate antimicrobial treatment may potentiate the progression from intermittent to chronic infection and also the emergence of antibiotic resistance. A better comprehension of the pathophysiology of PA infections and its implications for BE is urgently needed. This can drive improvements in diagnostic accuracy, can move us toward a new consensus definition of chronic infection, can better define the follow-up of patients at risk of PA, and can achieve more successful eradication rates. In addition, the new technological advances regarding molecular diagnostics, -omics, and biomarkers require us to reconsider our traditional concepts.

Keywords

bronchiectasis - Pseudomonas aeruginosa - biofilm - exacerbation - microbiome

Full Text

References

References
1 McShane PJ, Naureckas ET, Tino G, Strek ME. Non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med 2013; 188 (06) 647-656
2 Lonni S, Chalmers JD, Goeminne PC. et al. Etiology of non-cystic fibrosis bronchiectasis in adults and its correlation to disease severity. Ann Am Thorac Soc 2015; 12 (12) 1764-1770
3 Gavazzi G, Krause KH. Ageing and infection. Lancet Infect Dis 2002; 2 (11) 659-666
4 Chandrasekaran R, Mac Aogáin M, Chalmers JD, Elborn SJ, Chotirmall SH. Geographic variation in the aetiology, epidemiology and microbiology of bronchiectasis. BMC Pulm Med 2018; 18 (01) 83
5 Dimakou K, Triantafillidou C, Toumbis M, Tsikritsaki K, Malagari K, Bakakos P. Non CF-bronchiectasis: aetiologic approach, clinical, radiological, microbiological and functional profile in 277 patients. Respir Med 2016; 116: 1-7
6 King PT, Holdsworth SR, Freezer NJ, Villanueva E, Holmes PW. Microbiologic follow-up study in adult bronchiectasis. Respir Med 2007; 101 (08) 1633-1638
7 Munro KA, Reed PW, Joyce H. et al. Do New Zealand children with non-cystic fibrosis bronchiectasis show disease progression?. Pediatr Pulmonol 2011; 46 (02) 131-138
8 McDonnell MJ, Jary HR, Perry A. et al. Non cystic fibrosis bronchiectasis: a longitudinal retrospective observational cohort study of Pseudomonas persistence and resistance. Respir Med 2015; 109 (06) 716-726
9 Evans SA, Turner SM, Bosch BJ, Hardy CC, Woodhead MA. Lung function in bronchiectasis: the influence of Pseudomonas aeruginosa . Eur Respir J 1996; 9 (08) 1601-1604
10 Davies G, Wells AU, Doffman S, Watanabe S, Wilson R. The effect of Pseudomonas aeruginosa on pulmonary function in patients with bronchiectasis. Eur Respir J 2006; 28 (05) 974-979
11 Martínez-García MA, Soler-Cataluña J-J, Perpiñá-Tordera M, Román-Sánchez P, Soriano J. Factors associated with lung function decline in adult patients with stable non-cystic fibrosis bronchiectasis. Chest 2007; 132 (05) 1565-1572
12 Nicotra MB, Rivera M, Dale AM, Shepherd R, Carter R. Clinical, pathophysiologic, and microbiologic characterization of bronchiectasis in an aging cohort. Chest 1995; 108 (04) 955-961
13 Pasteur MC, Helliwell SM, Houghton SJ. et al. An investigation into causative factors in patients with bronchiectasis. Am J Respir Crit Care Med 2000; 162 (4, Pt 1): 1277-1284
14 Angrill J, Agustí C, de Celis R. et al. Bacterial colonisation in patients with bronchiectasis: microbiological pattern and risk factors. Thorax 2002; 57 (01) 15-19
15 Tunney MM, Einarsson GG, Wei L. et al. Lung microbiota and bacterial abundance in patients with bronchiectasis when clinically stable and during exacerbation. Am J Respir Crit Care Med 2013; 187 (10) 1118-1126
16 Menéndez R, Méndez R, Amara-Elori I. et al. Systemic inflammation during and after bronchiectasis exacerbations: impact of Pseudomonas aeruginosa . J Clin Med 2020; 9 (08) 2631
17 Aliberti S, Lonni S, Dore S. et al. Clinical phenotypes in adult patients with bronchiectasis. Eur Respir J 2016; 47 (04) 1113-1122
18 Martínez-García MA, Vendrell M, Girón R. et al. The multiple faces of non-cystic fibrosis bronchiectasis a cluster analysis approach. Ann Am Thorac Soc 2016; 13 (09) 1468-1475
19 Høiby N, Mathiesen L. Pseudomonas aeruginosa infection in cystic fibrosis. Distribution of B and T lymphocytes in relation to the humoral immune response. Acta Pathol Microbiol Scand B Microbiol Immunol 1974; 82 (04) 559-566
20 Hoiby N. Pseudomonas aeruginosa infection in cystic fibrosis. Diagnostic and prognostic significance of Pseudomonas aeruginosa precipitins determined by means of crossed immunoelectrophoresis. A survey. Acta Pathol Microbiol Scand Suppl 1977; (262) 1-96
21 Miszkiel KA, Wells AU, Rubens MB, Cole PJ, Hansell DM. Effects of airway infection by Pseudomonas aeruginosa: a computed tomographic study. Thorax 1997; 52 (03) 260-264
22 Wilson CB, Jones PW, O'Leary CJ, Hansell DM, Cole PJ, Wilson R. Effect of sputum bacteriology on the quality of life of patients with bronchiectasis. Eur Respir J 1997; 10 (08) 1754-1760
23 Polverino E, Goeminne PC, McDonnell MJ. et al. European Respiratory Society guidelines for the management of adult bronchiectasis. Eur Respir J 2017; 50 (03) 1700629
24 Finch S, McDonnell MJ, Abo-Leyah H, Aliberti S, Chalmers JD. A comprehensive analysis of the impact of Pseudomonas aeruginosa colonization on prognosis in adult bronchiectasis. Ann Am Thorac Soc 2015; 12 (11) 1602-1611
25 Gallego M, Pomares X, Espasa M. et al. Pseudomonas aeruginosa isolates in severe chronic obstructive pulmonary disease: characterization and risk factors. BMC Pulm Med 2014; 14 (01) 103
26 Suarez-Cuartin G, Smith A, Abo-Leyah H. et al. Anti-Pseudomonas aeruginosa IgG antibodies and chronic airway infection in bronchiectasis. Respir Med 2017; 128: 1-6
27 Lee SH, Lee Y, Park JS. et al. Characterization of microbiota in bronchiectasis patients with different disease severities. J Clin Med 2018; 7 (11) 429
28 Woo TE, Lim R, Heirali AA. et al. A longitudinal characterization of the non-cystic fibrosis bronchiectasis airway microbiome. Sci Rep 2019; 9 (01) 6871
29 Rogers GB, Bruce KD, Martin ML, Burr LD, Serisier DJ. The effect of long-term macrolide treatment on respiratory microbiota composition in non-cystic fibrosis bronchiectasis: an analysis from the randomised, double-blind, placebo-controlled BLESS trial. Lancet Respir Med 2014; 2 (12) 988-996
30 Høiby N, Frederiksen B, Pressler T. Eradication of early Pseudomonas aeruginosa infection. J Cyst Fibros 2005; 4 (02, Suppl 2): 49-54
31 Bartell JA, Sommer LM, Marvig RL. et al. Omics-based tracking of Pseudomonas aeruginosa persistence in “eradicated” CF patients. Eur Respir J 2021; 57 (04) 2000512
32 Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284 (5418): 1318-1322
33 Proesmans M, Balinska-Miskiewicz W, Dupont L. et al. Evaluating the “Leeds criteria” for Pseudomonas aeruginosa infection in a cystic fibrosis centre. Eur Respir J 2006; 27 (05) 937-943
34 Candido Caçador N, Paulino da Costa Capizzani C, Gomes Monteiro Marin Torres LA. et al. Adaptation of Pseudomonas aeruginosa to the chronic phenotype by mutations in the algTmucABD operon in isolates from Brazilian cystic fibrosis patients. PLoS One 2018; 13 (11) e0208013
35 Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu Rev Microbiol 2002; 56: 187-209
36 Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol 2007; 5 (01) 48-56
37 Høiby N, Bjarnsholt T, Moser C. et al; ESCMID Study Group for Biofilms and Consulting External Expert Werner Zimmerli. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014. Clin Microbiol Infect 2015; 21 (Suppl. 01) S1-S25
38 Marsh RL, Thornton RB, Smith-Vaughan HC, Richmond P, Pizzutto SJ, Chang AB. Detection of biofilm in bronchoalveolar lavage from children with non-cystic fibrosis bronchiectasis. Pediatr Pulmonol 2015; 50 (03) 284-292
39 Folkesson A, Jelsbak L, Yang L. et al. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 2012; 10 (12) 841-851
40 Martinez-García MA, Oscullo G, Posadas T. et al; Spanish Registry of Bronchiectasis Group of SEPAR (RIBRON). Pseudomonas aeruginosa and lung function decline in patients with bronchiectasis. Clin Microbiol Infect 2021; 27 (03) 428-434
41 Park J, Kim S, Lee YJ. et al. Factors associated with radiologic progression of non-cystic fibrosis bronchiectasis during long-term follow-up. Respirology 2016; 21 (06) 1049-1054
42 Chalmers JD, Smith MP, McHugh BJ, Doherty C, Govan JR, Hill AT. Short- and long-term antibiotic treatment reduces airway and systemic inflammation in non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med 2012; 186 (07) 657-665
43 Araújo D, Shteinberg M, Aliberti S. et al. The independent contribution of Pseudomonas aeruginosa infection to long-term clinical outcomes in bronchiectasis. Eur Respir J 2018; 51 (02) 1701953
44 Wang H, Ji X-B, Mao B, Li C-W, Lu H-W, Xu J-F. Pseudomonas aeruginosa isolation in patients with non-cystic fibrosis bronchiectasis: a retrospective study. BMJ Open 2018; 8 (03) e014613
45 de la Rosa D, Martínez-Garcia MA, Olveira C, Girón R, Máiz L, Prados C. Annual direct medical costs of bronchiectasis treatment: impact of severity, exacerbations, chronic bronchial colonization and chronic obstructive pulmonary disease coexistence. Chron Respir Dis 2016; 13 (04) 361-371
46 Garcia-Clemente M, de la Rosa D, Máiz L. et al. Impact of Pseudomonas aeruginosa infection on patients with chronic inflammatory airway diseases. J Clin Med 2020; 9 (12) 3800
47 Chalmers JD, Goeminne P, Aliberti S. et al. The bronchiectasis severity index: an international derivation and validation study. Am J Respir Crit Care Med 2014; 189 (05) 576-585
48 Martínez-García MA, de Gracia J, Vendrell Relat M. et al. Multidimensional approach to non-cystic fibrosis bronchiectasis: the FACED score. Eur Respir J 2014; 43 (05) 1357-1367
49 Alcaraz-Serrano V, Fernández-Barat L, Scioscia G. et al. Mucoid Pseudomonas aeruginosa alters sputum viscoelasticity in patients with non-cystic fibrosis bronchiectasis. Respir Med 2019; 154 (May): 40-46
50 Murray PR, Washington JA. Microscopic and baceriologic analysis of expectorated sputum. Mayo Clin Proc 1975; 50 (06) 339-344
51 Camoez M, Sierra JM, Dominguez MA, Ferrer-Navarro M, Vila J, Roca I. Automated categorization of methicillin-resistant Staphylococcus aureus clinical isolates into different clonal complexes by MALDI-TOF mass spectrometry. Clin Microbiol Infect 2016; 22 (02) 161.e1-161.e7
52 Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 2003; 57: 677-701
53 Hall-Stoodley L, Stoodley P, Kathju S. et al. Towards diagnostic guidelines for biofilm-associated infections. FEMS Immunol Med Microbiol 2012; 65 (02) 127-145
54 Trampuz A, Piper KE, Jacobson MJ. et al. Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 2007; 357 (07) 654-663
55 Fernández-Barat L, Ciofu O, Kragh KN. et al. Phenotypic shift in Pseudomonas aeruginosa populations from cystic fibrosis lungs after 2-week antipseudomonal treatment. J Cyst Fibros 2017; 16 (02) 222-229
56 Webber DM, Wallace MA, Burnham CAD, Anderson NW. Evaluation of the BioFire FilmArray Pneumonia Panel for detection of viral and bacterial pathogens in lower respiratory tract specimens in the setting of a tertiary care academic medical center. J Clin Microbiol 2020; 58 (07) e00343-20
57 Rand KH, Beal SG, Cherabuddi K. et al. Performance of a semiquantitative multiplex bacterial and viral PCR panel compared with standard microbiological laboratory results: 396 patients studied with the BioFire Pneumonia Panel. Open Forum Infect Dis 2020; 8 (01) a560
58 Murphy CN, Fowler R, Balada-Llasat JM. et al. Multicenter evaluation of the BioFire FilmArray Pneumonia/Pneumonia Plus Panel for detection and quantification of agents of lower respiratory tract infection. J Clin Microbiol 2020; 58 (07) e00128-20
59 Buchan BW, Windham S, Balada-Llasat JM. et al. Practical comparison of the BioFire FilmArray pneumonia panel to routine diagnostic methods and potential impact on antimicrobial stewardship in adult hospitalized patients with lower respiratory tract infections. J Clin Microbiol 2020; 58 (07) e00135-20
60 Mandell LA, Wunderink RG, Anzueto A. et al; Infectious Diseases Society of America, American Thoracic Society. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis 2007; 44 (Suppl. 02) S27-S72
61 Whitters D, Stockley R. Immunity and bacterial colonisation in bronchiectasis. Thorax 2012; 67 (11) 1006-1013
62 Cullen L, McClean S. Bacterial adaptation during chronic respiratory infections. Pathogens 2015; 4 (01) 66-89
63 Chalmers JD, Hill AT. Mechanisms of immune dysfunction and bacterial persistence in non-cystic fibrosis bronchiectasis. Mol Immunol 2013; 55 (01) 27-34
64 Hill AT, Sullivan AL, Chalmers JD. et al. British thoracic society guideline for bronchiectasis in adults. Thorax 2019; 74 (Suppl. 01) 1-69
65 Vallières E, Tumelty K, Tunney MM. et al. Efficacy of Pseudomonas aeruginosa eradication regimens in bronchiectasis. Eur Respir J 2017; 49 (04) 1600851
66 Orriols R, Hernando R, Ferrer A, Terradas S, Montoro B. Eradication therapy against Pseudomonas aeruginosa in non-cystic fibrosis bronchiectasis. Respiration 2015; 90 (04) 299-305
67 Bell SC, Elborn JS, Byrnes CA. Bronchiectasis: treatment decisions for pulmonary exacerbations and their prevention. Respirology 2018; 23 (11) 1006-1022
68 Chalmers JD, Moffitt KL, Suarez-Cuartin G. et al. Neutrophil elastase activity is associated with exacerbations and lung function decline in bronchiectasis. Am J Respir Crit Care Med 2017; 195 (10) 1384-1393
69 Courtney JM, Kelly MG, Watt A. et al. Quality of life and inflammation in exacerbations of bronchiectasis. Chron Respir Dis 2008; 5 (03) 161-168
70 Hodge G, Upham JW, Chang AB. et al. Increased peripheral blood pro-inflammatory/cytotoxic lymphocytes in children with bronchiectasis. PLoS One 2015; 10 (08) e0133695
71 Kapur N, Grimwood K, Masters IB, Morris PS, Chang AB. Lower airway microbiology and cellularity in children with newly diagnosed non-CF bronchiectasis. Pediatr Pulmonol 2012; 47 (03) 300-307
72 Quittner AL, O'Donnell AE, Salathe MA. et al. Quality of Life Questionnaire-Bronchiectasis: final psychometric analyses and determination of minimal important difference scores. Thorax 2015; 70 (01) 12-20
73 Hill AT, Haworth CS, Aliberti S. et al; EMBARC/BRR Definitions Working Group. Pulmonary exacerbation in adults with bronchiectasis: a consensus definition for clinical research. Eur Respir J 2017; 49 (06) 1700051
74 Martínez-García MÁ, Máiz L, Olveira C. et al. Normativa sobre el tratamiento de las bronquiectasias en el adulto. Arch Bronconeumol 2018; 54 (02) 88-98
75 Wilson R, Aksamit T, Aliberti S. et al. Challenges in managing Pseudomonas aeruginosa in non-cystic fibrosis bronchiectasis. Respir Med 2016; 117: 179-189
76 King PT, Holdsworth SR, Freezer NJ, Villanueva E, Holmes PW. Characterisation of the onset and presenting clinical features of adult bronchiectasis. Respir Med 2006; 100 (12) 2183-2189
77 Basavaraj A, Choate R, Addrizzo-Harris D. et al. Airway clearance techniques in bronchiectasis: analysis from the United States Bronchiectasis and Non-TB Mycobacteria Research Registry. Chest 2020; 158 (04) 1376-1384
78 Lee AL, Burge AT, Holland AE. Airway clearance techniques for bronchiectasis. Cochrane Database Syst Rev 2015; 2015 (11) CD008351
79 King PT. Pseudomonas aeruginosa cross-infection: Is this important in bronchiectasis and COPD?. Respirology 2019; 24 (10) 926-927
80 Herrero Cortina B, Aliberti S, Blasi F. et al. Chest physiotherapy in European patients with bronchiectasis: data from the EMBARC registry. Eur Respir J 2017; 50 (Suppl. 61) PA4071
81 Alcaraz-Serrano V, Gimeno-Santos E, Scioscia G. et al. Association between physical activity and risk of hospitalisation in bronchiectasis. Eur Respir J 2020; 55 (06) 1-9
82 Fernández-Barat L, López-Aladid R, Torres A. Reconsidering ventilator-associated pneumonia from a new dimension of the lung microbiome. EBioMedicine 2020; 60: 102995
83 Dickson RP, Erb-Downward JR, Huffnagle GB. Towards an ecology of the lung: new conceptual models of pulmonary microbiology and pneumonia pathogenesis. Lancet Respir Med 2014; 2 (03) 238-246
84 Cox MJ, Turek EM, Hennessy C. et al. Longitudinal assessment of sputum microbiome by sequencing of the 16S rRNA gene in non-cystic fibrosis bronchiectasis patients. PLoS One 2017; 12 (02) e0170622
85 Rogers GB, Zain NMM, Bruce KD. et al. A novel microbiota stratification system predicts future exacerbations in bronchiectasis. Ann Am Thorac Soc 2014; 11 (04) 496-503
86 Taylor SL, Woodman RJ, Chen AC. et al. FUT2 genotype influences lung function, exacerbation frequency and airway microbiota in non-CF bronchiectasis. Thorax 2017; 72 (04) 304-310
87 Richardson H, Dicker AJ, Barclay H, Chalmers JD. The microbiome in bronchiectasis. Eur Respir Rev 2019; 28 (153) 190048
88 He X, Hu W, He J, Guo L, Lux R, Shi W. Community-based interference against integration of Pseudomonas aeruginosa into human salivary microbial biofilm. Mol Oral Microbiol 2011; 26 (06) 337-352
89 Li L, Zhang J, Li Z. et al. Airway microbiota is associated with the severity of non-CF bronchiectasis. Clin Respir J 2021; 15 (02) 154-162
90 Voynow JA, Gendler SJ, Rose MC. Regulation of mucin genes in chronic inflammatory airway diseases. Am J Respir Cell Mol Biol 2006; 34 (06) 661-665
91 Williams OW, Sharafkhaneh A, Kim V, Dickey BF, Evans CM. Airway mucus: from production to secretion. Am J Respir Cell Mol Biol 2006; 34 (05) 527-536
92 Lai SK, Wang YY, Wirtz D, Hanes J. Micro- and macrorheology of mucus. Adv Drug Deliv Rev 2009; 61 (02) 86-100
93 Rogers SS, van der Walle C, Waigh TA. Microrheology of bacterial biofilms in vitro: Staphylococcus aureus and Pseudomonas aeruginosa . Langmuir 2008; 24 (23) 13549-13555
94 Gloag ES, German GK, Stoodley P, Wozniak DJ. Viscoelastic properties of Pseudomonas aeruginosa variant biofilms. Sci Rep 2018; 8 (01) 9691
95 Murgia X, Kany AM, Herr C. et al. Micro-rheological properties of lung homogenates correlate with infection severity in a mouse model of Pseudomonas aeruginosa lung infection. Sci Rep 2020; 10 (01) 16502