Biofilm infections of endobronchial valves in COPD patients after endoscopic lung volume reduction: a pilot study with FISHseq.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
04 Oct 2024
Historique:
received: 22 04 2024
accepted: 23 09 2024
medline: 5 10 2024
pubmed: 5 10 2024
entrez: 4 10 2024
Statut: epublish

Résumé

Endoscopic lung volume reduction (ELVR) using endobronchial valves (EBV) is a treatment option for a subset of patients with severe chronic obstructive pulmonary disease (COPD), suffering from emphysema and hyperinflation. In this pilot study, we aimed to determine the presence of bacterial biofilm infections on EBV and investigate their involvement in lack of clinical benefits, worsening symptomatology, and increased exacerbations that lead to the decision to remove EBVs. We analyzed ten COPD patients with ELVR who underwent EBV removal. Clinical data were compared to the microbiological findings from conventional EBV culture. In addition, EBV were analyzed by FISHseq, a combination of Fluorescence in situ hybridization (FISH) with PCR and sequencing, for visualization and identification of microorganisms and biofilms. All ten patients presented with clinical symptoms, including pneumonia and recurrent exacerbations. Microbiological cultures from EBV detected several microorganisms in all ten patients. FISHseq showed either mixed or monospecies colonization on the EBV, including oropharyngeal bacterial flora, Staphylococcus aureus, Pseudomonas aeruginosa, Streptococcus spp., and Fusobacterium sp. On 5/10 EBV, FISHseq visualized biofilms, on 1/10 microbial microcolonies, on 3/10 single microorganisms, and on 1/10 no microorganisms. The results of the study demonstrate the presence of biofilms on EBV for the first time and its potential involvement in increased exacerbations and clinical worsening in patients with ELVR. However, further prospective studies are needed to evaluate the clinical relevance of biofilm formation on EBV and appropriate treatment options to avoid infections in patients with ELVR.

Identifiants

pubmed: 39366990
doi: 10.1038/s41598-024-73950-3
pii: 10.1038/s41598-024-73950-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

23078

Informations de copyright

© 2024. The Author(s).

Références

Adeloye, D. et al. Global, regional, and national prevalence of, and risk factors for, chronic obstructive pulmonary disease (COPD) in 2019: A systematic review and modelling analysis. Lancet Respir. Med.10, 447–458. https://doi.org/10.1016/S2213-2600(21)00511-7 (2022).
doi: 10.1016/S2213-2600(21)00511-7 pubmed: 35279265 pmcid: 9050565
Lin, C. R., Bahmed, K. & Kosmider, B. Dysregulated cell signaling in pulmonary emphysema. Front. Med. (Lausanne)8, 762878. https://doi.org/10.3389/fmed.2021.762878 (2021).
doi: 10.3389/fmed.2021.762878 pubmed: 35047522
Slebos, D. J., Shah, P. L., Herth, F. J. & Valipour, A. Endobronchial valves for endoscopic lung volume reduction: Best practice recommendations from expert panel on endoscopic lung volume reduction. Respiration93, 138–150. https://doi.org/10.1159/000453588 (2017).
doi: 10.1159/000453588 pubmed: 27992862
Davey, C. et al. Bronchoscopic lung volume reduction with endobronchial valves for patients with heterogeneous emphysema and intact interlobar fissures (the BeLieVeR-HIFi study): A randomised controlled trial. Lancet386, 1066–1073. https://doi.org/10.1016/S0140-6736(15)60001-0 (2015).
doi: 10.1016/S0140-6736(15)60001-0 pubmed: 26116485
Herth, F. J. et al. Efficacy predictors of lung volume reduction with Zephyr valves in a European cohort. Eur. Respir. J.39, 1334–1342. https://doi.org/10.1183/09031936.00161611 (2012).
doi: 10.1183/09031936.00161611 pubmed: 22282552
Sciurba, F. C. et al. A randomized study of endobronchial valves for advanced emphysema. N. Engl. J. Med.363, 1233–1244. https://doi.org/10.1056/NEJMoa0900928 (2010).
doi: 10.1056/NEJMoa0900928 pubmed: 20860505
Hubner, R. H. et al. Endoscopic lung volume reduction: Can endobronchial valves be safely removed? Respiration99, 459–460. https://doi.org/10.1159/000506522 (2020).
doi: 10.1159/000506522 pubmed: 32200375
Wedzicha, J. A. & Seemungal, T. A. COPD exacerbations: Defining their cause and prevention. Lancet370, 786–796. https://doi.org/10.1016/S0140-6736(07)61382-8 (2007).
doi: 10.1016/S0140-6736(07)61382-8 pubmed: 17765528 pmcid: 7134993
Hurst, J. R., Perera, W. R., Wilkinson, T. M., Donaldson, G. C. & Wedzicha, J. A. Systemic and upper and lower airway inflammation at exacerbation of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.173, 71–78. https://doi.org/10.1164/rccm.200505-704OC (2006).
doi: 10.1164/rccm.200505-704OC pubmed: 16179639
Donaldson, G. C., Seemungal, T. A. R., Bhowmik, A. & Wedzicha, J. A. Relationship between exacerbation frequency and lung function decline in chronic obstructive pulmonary disease. Thorax57, 847–852. https://doi.org/10.1136/thorax.57.10.847 (2002).
doi: 10.1136/thorax.57.10.847 pubmed: 12324669 pmcid: 1746193
Seemungal, T. A. et al. Effect of exacerbation on quality of life in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.157, 1418–1422. https://doi.org/10.1164/ajrccm.157.5.9709032 (1998).
doi: 10.1164/ajrccm.157.5.9709032 pubmed: 9603117
Soler-Cataluña, J. J. et al. Severe acute exacerbations and mortality in patients with chronic obstructive pulmonary disease. Thorax60, 925–931. https://doi.org/10.1136/thx.2005.040527 (2005).
doi: 10.1136/thx.2005.040527 pubmed: 16055622 pmcid: 1747235
Ball, P. & 43S-52S. Epidemiology and treatment of chronic bronchitis and its exacerbations. CHEST108 (1995). https://doi.org/10.1378/chest.108.2_Supplement.43S
Bouquet, J. et al. Microbial burden and viral exacerbations in a longitudinal multicenter COPD cohort. Respir Res.21, 77. https://doi.org/10.1186/s12931-020-01340-0 (2020).
doi: 10.1186/s12931-020-01340-0 pubmed: 32228581 pmcid: 7104712
Patel, I. S. et al. Relationship between bacterial colonisation and the frequency, character, and severity of COPD exacerbations. Thorax57, 759–764. https://doi.org/10.1136/thorax.57.9.759 (2002).
doi: 10.1136/thorax.57.9.759 pubmed: 12200518 pmcid: 1746426
Weeks, J. R., Staples, K. J., Spalluto, C. M., Watson, A. & Wilkinson, T. M. A. The role of non-typeable haemophilus influenzae biofilms in chronic obstructive pulmonary disease. Front. Cell. Infect. Microbiol.11, 720742. https://doi.org/10.3389/fcimb.2021.720742 (2021).
doi: 10.3389/fcimb.2021.720742 pubmed: 34422683 pmcid: 8373199
Donlan, R. M. Biofilms and device-associated infections. Emerg. Infect. Dis.7, 277–281. https://doi.org/10.3201/eid0702.010226 (2001).
doi: 10.3201/eid0702.010226 pubmed: 11294723 pmcid: 2631701
Stewart, P. S. & Costerton, J. W. Antibiotic resistance of bacteria in biofilms. Lancet358, 135–138. https://doi.org/10.1016/s0140-6736(01)05321-1 (2001).
doi: 10.1016/s0140-6736(01)05321-1 pubmed: 11463434
Xu, Y. et al. Microbiological diagnosis of device-related biofilm infections. Apmis125, 289–303. https://doi.org/10.1111/apm.12676 (2017).
doi: 10.1111/apm.12676 pubmed: 28407422
Fruchter, O. et al. Airway bacterial colonization and serum C-reactive protein are associated with chronic obstructive pulmonary disease exacerbation following bronchoscopic lung volume reduction. Clin. Respir. J.10, 239–245. https://doi.org/10.1111/crj.12211 (2016).
doi: 10.1111/crj.12211 pubmed: 25196428
Lenga, P. et al. Endoscopic lung volume reduction with endobronchial valves in very low D (LCO) patients: Results from the German Registry - Lungenemphysemregister e.V. ERJ Open. Res.7. https://doi.org/10.1183/23120541.00449-2020 (2021).
Lefmann, M. et al. Evaluation of peptide nucleic acid-fluorescence in situ hybridization for identification of clinically relevant mycobacteria in clinical specimens and tissue sections. J. Clin. Microbiol.44, 3760–3767. https://doi.org/10.1128/jcm.01435-06 (2006).
doi: 10.1128/jcm.01435-06 pubmed: 17021106 pmcid: 1594750
Mallmann, C. et al. Fluorescence in situ hybridization to improve the diagnosis of endocarditis: A pilot study. Clin. Microbiol. Infect.16, 767–773. https://doi.org/10.1111/j.1469-0691.2009.02936.x (2010).
doi: 10.1111/j.1469-0691.2009.02936.x pubmed: 19694763
Hajduczenia, M. M. et al. New perspectives for prosthetic valve endocarditis: Impact of molecular imaging by FISHseq diagnostics. Clin. Infect. Dis.76, 1050–1058. https://doi.org/10.1093/cid/ciac860 (2023).
doi: 10.1093/cid/ciac860 pubmed: 36318608
Amann, R. I. et al. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol.56, 1919–1925 (1990).
doi: 10.1128/aem.56.6.1919-1925.1990 pubmed: 2200342 pmcid: 184531
Wallner, G., Amann, R. & Beisker, W. Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry14, 136–143. https://doi.org/10.1002/cyto.990140205 (1993).
doi: 10.1002/cyto.990140205 pubmed: 7679962
Schoenrath, F. et al. Fluorescence in situ hybridization and polymerase chain reaction to detect infections in patients with Left Ventricular Assist devices. ASAIO J.67 (2021).
Gescher, D. M. et al. Fluorescence in situ hybridisation (FISH) accelerates identification of gram-positive cocci in positive blood cultures. Int. J. Antimicrob. Agents32(Suppl 1), 51–59. https://doi.org/10.1016/j.ijantimicag.2008.06.007 (2008).
doi: 10.1016/j.ijantimicag.2008.06.007
Kikhney, J. & Moter, A. Quality control in diagnostic fluorescence in situ hybridization (FISH) in microbiology. Methods Mol. Biol.2246, 301–316. https://doi.org/10.1007/978-1-0716-1115-9_20 (2021).
doi: 10.1007/978-1-0716-1115-9_20 pubmed: 33576998
Sutrave, S. et al. Effect of daptomycin and vancomycin on Staphylococcus epidermidis biofilms: An in vitro assessment using fluorescence in situ hybridization. PLoS One14, e0221786. https://doi.org/10.1371/journal.pone.0221786 (2019).
doi: 10.1371/journal.pone.0221786 pubmed: 31454398 pmcid: 6711592
Hsieh, K., Mach, K. E., Zhang, P., Liao, J. C. & Wang, T. H. Combating antimicrobial resistance via single-cell diagnostic technologies powered by droplet microfluidics. Acc. Chem. Res.55, 123–133. https://doi.org/10.1021/acs.accounts.1c00462 (2022).
doi: 10.1021/acs.accounts.1c00462 pubmed: 34898173
Church, D. L. et al. Performance and application of 16S rRNA gene cycle sequencing for routine identification of bacteria in the clinical microbiology laboratory. Clin. Microbiol. Rev.33. https://doi.org/10.1128/cmr.00053-19 (2020).
Agrafiotis, M., Siempos, I. I. & Falagas, M. E. Infections related to airway stenting: A systematic review. Respiration78, 69–74. https://doi.org/10.1159/000213244 (2009).
doi: 10.1159/000213244 pubmed: 19365108
Rosell, A. et al. Microbiologic determinants of exacerbation in chronic obstructive pulmonary disease. Arch. Intern. Med.165, 891–897. https://doi.org/10.1001/archinte.165.8.891 (2005).
doi: 10.1001/archinte.165.8.891 pubmed: 15851640
Hall-Stoodley, L. et al. Towards diagnostic guidelines for biofilm-associated infections. FEMS Immunol. Med. Microbiol.65, 127–145. https://doi.org/10.1111/j.1574-695X.2012.00968.x (2012).
doi: 10.1111/j.1574-695X.2012.00968.x pubmed: 22469292
Sarmand, N. et al. New bacterial growth in bronchial secretions after bronchoscopic valve implantation. Int. J. Chron. Obstruct Pulmon Dis.13, 565–570. https://doi.org/10.2147/COPD.S148196 (2018).
doi: 10.2147/COPD.S148196 pubmed: 29445273 pmcid: 5810521
Noppen, M., Pierard, D., Meysman, M., Claes, I. & Vincken, W. Bacterial colonization of central airways after stenting. Am. J. Respir. Crit. Care Med.160, 672–677. https://doi.org/10.1164/ajrccm.160.2.9812081 (1999).
doi: 10.1164/ajrccm.160.2.9812081 pubmed: 10430745
Eklof, J. et al. Pseudomonas aeruginosa and risk of death and exacerbations in patients with chronic obstructive pulmonary disease: An observational cohort study of 22 053 patients. Clin. Microbiol. Infect.26, 227–234. https://doi.org/10.1016/j.cmi.2019.06.011 (2020).
doi: 10.1016/j.cmi.2019.06.011 pubmed: 31238116
Kolpen, M. et al. Bacterial biofilms predominate in both acute and chronic human lung infections. Thorax77, 1015–1022. https://doi.org/10.1136/thoraxjnl-2021-217576 (2022).
doi: 10.1136/thoraxjnl-2021-217576 pubmed: 35017313
Klooster, K. & Slebos, D. J. Endobronchial valves for the treatment of advanced emphysema. Chest159, 1833–1842. https://doi.org/10.1016/j.chest.2020.12.007 (2021).
doi: 10.1016/j.chest.2020.12.007 pubmed: 33345947
Klooster, K. et al. Endobronchial valves for emphysema without interlobar collateral ventilation. N. Engl. J. Med.373, 2325–2335. https://doi.org/10.1056/NEJMoa1507807 (2015).
doi: 10.1056/NEJMoa1507807 pubmed: 26650153
Valipour, A. et al. Endobronchial valve therapy in patients with homogeneous emphysema. Results from the IMPACT Study. Am. J. Respir Crit. Care Med.194, 1073–1082. https://doi.org/10.1164/rccm.201607-1383OC (2016).
doi: 10.1164/rccm.201607-1383OC pubmed: 27580428
Kemp, S. V. et al. A multicenter randomized controlled trial of zephyr endobronchial valve treatment in heterogeneous emphysema (TRANSFORM). Am. J. Respir. Crit. Care Med.196, 1535–1543. https://doi.org/10.1164/rccm.201707-1327OC (2017).
doi: 10.1164/rccm.201707-1327OC pubmed: 28885054
Criner, G. J. et al. A multicenter randomized controlled trial of zephyr endobronchial valve treatment in heterogeneous emphysema (LIBERATE). Am. J. Respir. Crit. Care Med.198, 1151–1164. https://doi.org/10.1164/rccm.201803-0590OC (2018).
doi: 10.1164/rccm.201803-0590OC pubmed: 29787288
Conway, F. et al. A retrospective analysis assessing prevalence of microbes in patients undergoing endobronchial valve (EBV) insertion for chronic obstructive pulmonary disease (COPD). Eur. Respir. J.62, PA5224. https://doi.org/10.1183/13993003.congress-2023.PA5224 (2023).
doi: 10.1183/13993003.congress-2023.PA5224
Pawar, V. et al. In vivo efficacy of antimicrobials against biofilm-producing pseudomonas aeruginosa. Antimicrob. Agents Chemother.59, 4974–4981. https://doi.org/10.1128/aac.00194-15 (2015).
doi: 10.1128/aac.00194-15 pubmed: 26055372 pmcid: 4505208
Loy, A., Horn, M. & Wagner, M. probeBase: An online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res.31, 514–516. https://doi.org/10.1093/nar/gkg016 (2003).
doi: 10.1093/nar/gkg016 pubmed: 12520066 pmcid: 165463

Auteurs

Eva Pappe (E)

Department of Infectious Disease, Respiratory Medicine and Critical Care, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany. eva.pappe@charite.de.

Ralf-Harto Hübner (RH)

Department of Infectious Disease, Respiratory Medicine and Critical Care, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.

Jacopo Saccomanno (J)

Department of Infectious Disease, Respiratory Medicine and Critical Care, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.

Hadis Darvishi Nakhl Ebrahimi (HDN)

Department of Infectious Disease, Respiratory Medicine and Critical Care, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.

Martin Witzenrath (M)

Department of Infectious Disease, Respiratory Medicine and Critical Care, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.
German Center for Lung Research (DZL), Berlin, Germany.
Capnetz Foundation, Hannover, Germany.

Alexandra Wiessner (A)

Institute of Microbiology, Infectious Diseases and Immunology, Biofilmcenter, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.
MoKi Analytics GmbH, Berlin, Germany.

Kurosh Sarbandi (K)

Institute of Microbiology, Infectious Diseases and Immunology, Biofilmcenter, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.

Zhile Xiong (Z)

Institute of Microbiology, Infectious Diseases and Immunology, Biofilmcenter, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.
MoKi Analytics GmbH, Berlin, Germany.

Laura Kursawe (L)

Institute of Microbiology, Infectious Diseases and Immunology, Biofilmcenter, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.

Annette Moter (A)

Institute of Microbiology, Infectious Diseases and Immunology, Biofilmcenter, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.
Moter Diagnostics, Berlin, Germany.

Judith Kikhney (J)

Institute of Microbiology, Infectious Diseases and Immunology, Biofilmcenter, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt- Universität zu Berlin, Hindenburgdamm 30, 12203, Berlin, Germany.
MoKi Analytics GmbH, Berlin, Germany.

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