Exploring alveolar recruitability using positive end-expiratory pressure in mice overexpressing TGF-β1: a structure-function analysis.

Acute respiratory distress syndrome Atelectasis Recruitment Stereology TGF-β1 Ventilation induced lung injury

Journal

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

Informations de publication

Date de publication:
06 Apr 2024
Historique:
received: 11 12 2023
accepted: 26 03 2024
medline: 7 4 2024
pubmed: 7 4 2024
entrez: 6 4 2024
Statut: epublish

Résumé

Pre-injured lungs are prone to injury progression in response to mechanical ventilation. Heterogeneous ventilation due to (micro)atelectases imparts injurious strains on open alveoli (known as volutrauma). Hence, recruitment of (micro)atelectases by positive end-expiratory pressure (PEEP) is necessary to interrupt this vicious circle of injury but needs to be balanced against acinar overdistension. In this study, the lung-protective potential of alveolar recruitment was investigated and balanced against overdistension in pre-injured lungs. Mice, treated with empty vector (AdCl) or adenoviral active TGF-β1 (AdTGF-β1) were subjected to lung mechanical measurements during descending PEEP ventilation from 12 to 0 cmH

Identifiants

pubmed: 38582767
doi: 10.1038/s41598-024-58213-5
pii: 10.1038/s41598-024-58213-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

8080

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : 471334884
Organisme : Bundesministerium für Bildung und Forschung
ID : German Center for Lung Research

Informations de copyright

© 2024. Crown.

Références

Bellani, G. et al. Epidemiology, Patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries. JAMA 315, 788–800 (2016).
pubmed: 26903337 doi: 10.1001/jama.2016.0291
Slutsky, A. S. & Ranieri, V. M. Ventilator-induced lung injury. N. Engl. J. Med. 370, 980 (2014).
pubmed: 24597883
Gaver, D. P. et al. The POOR get POORer: A hypothesis for the pathogenesis of ventilator-induced lung injury. Am. J. Respir. Crit. Care Med. 202, 1081–1087 (2020).
pubmed: 33054329 pmcid: 7560804 doi: 10.1164/rccm.202002-0453CP
Hamlington, K. L. et al. Alveolar leak develops by a rich-get-richer process in ventilator-induced lung injury. PLoS One 13, e0193934 (2018).
pubmed: 29590136 pmcid: 5874026 doi: 10.1371/journal.pone.0193934
Bilek, A. M., Dee, K. C. & Gaver, D. P. Mechanisms of surface-tension-induced epithelial cell damage in a model of pulmonary airway reopening. J. Appl. Physiol. 2003(94), 770–783 (1985).
Perlman, C. E. & Wu, Y. In situ determination of alveolar septal strain, stress and effective Young’s modulus: An experimental/computational approach. Am. J. Physiol. Lung Cell Mol. Physiol. 307, L302-310 (2014).
pubmed: 24951778 pmcid: 4137161 doi: 10.1152/ajplung.00106.2014
Gattinoni, L. & Pesenti, A. The concept of “baby lung”. Intensive Care Med. 31, 776–784 (2005).
pubmed: 15812622 doi: 10.1007/s00134-005-2627-z
Nieman, G. F. et al. Personalizing mechanical ventilation according to physiologic parameters to stabilize alveoli and minimize ventilator induced lung injury (VILI). Intensive Care Med. Exp. 5, 8 (2017).
pubmed: 28150228 pmcid: 5289131 doi: 10.1186/s40635-017-0121-x
Walkey, A. J. et al. Higher PEEP versus lower PEEP strategies for patients with acute respiratory distress syndrome. A systematic review and meta-analysis. Ann. Am. Thorac. Soc. 14, S297–S303 (2017).
pubmed: 29043834 doi: 10.1513/AnnalsATS.201704-338OT
Güldner, A. et al. Comparative effects of volutrauma and atelectrauma on lung inflammation in experimental acute respiratory distress syndrome. Crit. Care Med. 44, e854-865 (2016).
pubmed: 27035236 pmcid: 5105831 doi: 10.1097/CCM.0000000000001721
Bilodeaux, J. et al. Differential effects of two-hit models of acute and ventilator-induced lung injury on lung structure, function, and inflammation. Front. Physiol. 14, 1217183 (2023).
pubmed: 37565138 pmcid: 10410077 doi: 10.3389/fphys.2023.1217183
Smith, B. J. et al. Three alveolar phenotypes govern lung function in murine ventilator-induced lung injury. Front. Physiol. 11, 660 (2020).
pubmed: 32695013 pmcid: 7338482 doi: 10.3389/fphys.2020.00660
Nieman, G. F. et al. A physiologically informed strategy to effectively open, stabilize, and protect the acutely injured lung. Front. Physiol. 11, 227 (2020).
pubmed: 32265734 pmcid: 7096584 doi: 10.3389/fphys.2020.00227
Costa, E. L. et al. Bedside estimation of recruitable alveolar collapse and hyperdistension by electrical impedance tomography. Intensive Care Med. 35, 1132–1137 (2009).
pubmed: 19255741 doi: 10.1007/s00134-009-1447-y
Jonkman, A. H. et al. Lung recruitment assessed by electrical impedance tomography (RECRUIT): A multicenter study of COVID-19 acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 208, 25–38 (2023).
pubmed: 37097986 pmcid: 10870845 doi: 10.1164/rccm.202212-2300OC
Gattinoni, L. et al. Lung recruitment in patients with the acute respiratory distress syndrome. N. Engl. J. Med. 354, 1775–1786 (2006).
pubmed: 16641394 doi: 10.1056/NEJMoa052052
Cressoni, M. et al. Opening pressures and atelectrauma in acute respiratory distress syndrome. Intensive Care Med. 43, 603–611 (2017).
pubmed: 28283699 doi: 10.1007/s00134-017-4754-8
Sime, P. J., Xing, Z., Graham, F. L., Csaky, K. G. & Gauldie, J. Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J. Clin. Invest. 100, 768–776 (1997).
pubmed: 9259574 pmcid: 508247 doi: 10.1172/JCI119590
Ask, K. et al. Comparison between conventional and “clinical” assessment of experimental lung fibrosis. J. Transl. Med. 6, 16 (2008).
pubmed: 18402687 pmcid: 2365932 doi: 10.1186/1479-5876-6-16
Berg, J. T. et al. High lung inflation increases mRNA levels of ECM components and growth factors in lung parenchyma. J. Appl. Physiol. 1997(83), 120–128 (1985).
Correll, K. A. et al. TGF beta inhibits expression of SP-A, SP-B, SP-C, but not SP-D in human alveolar type II cells. Biochem. Biophys. Res. Commun. 499, 843–848 (2018).
pubmed: 29621540 pmcid: 6204198 doi: 10.1016/j.bbrc.2018.04.003
Lopez-Rodriguez, E. et al. Surfactant dysfunction during overexpression of TGF-β1 precedes profibrotic lung remodeling in vivo. Am. J. Physiol. Lung Cell Mol. Physiol. 310, L1260-1271 (2016).
pubmed: 27106287 doi: 10.1152/ajplung.00065.2016
Beike, L. et al. Surfactant dysfunction and alveolar collapse are linked with fibrotic septal wall remodeling in the TGF-β1-induced mouse model of pulmonary fibrosis. Lab. Invest. 99, 830–852 (2019).
pubmed: 30700849 doi: 10.1038/s41374-019-0189-x
Percie du Sert, N. et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. BMJ Open Sci. 4, e100115 (2020).
pubmed: 34095516 pmcid: 7610906
Hantos, Z., Daróczy, B., Suki, B., Nagy, S. & Fredberg, J. J. Input impedance and peripheral inhomogeneity of dog lungs. J. Appl. Physiol. 72, 168–178 (1992).
pubmed: 1537711 doi: 10.1152/jappl.1992.72.1.168
Fredberg, J. J. & Stamenovic, D. On the imperfect elasticity of lung tissue. J. Appl. Physiol. 1989(67), 2408–2419 (1985).
Lai, Y. L. & Chou, H. Respiratory mechanics and maximal expiratory flow in the anesthetized mouse. J. Appl. Physiol. 2000(88), 939–943 (1985).
Tschanz, S., Schneider, J. P. & Knudsen, L. Design-based stereology: Planning, volumetry and sampling are crucial steps for a successful study. Ann. Anat. 196, 3–11 (2014).
pubmed: 23769130 doi: 10.1016/j.aanat.2013.04.011
Mühlfeld, C., Knudsen, L. & Ochs, M. Stereology and morphometry of lung tissue. Methods Mol. Biol. 931, 367–390 (2013).
pubmed: 23027012 doi: 10.1007/978-1-62703-056-4_18
Gundersen, H. J. The smooth fractionator. J. Microsc. 207, 191–210 (2002).
pubmed: 12230489 doi: 10.1046/j.1365-2818.2002.01054.x
Cruz-Orive, L. M. & Weibel, E. R. Recent stereological methods for cell biology: A brief survey. Am. J. Physiol. 258, L148-156 (1990).
pubmed: 2185653
Rizzo, A. N. et al. Alveolar epithelial glycocalyx degradation mediates surfactant dysfunction and contributes to acute respiratory distress syndrome. JCI Insight 7, e154573 (2022).
pubmed: 34874923 pmcid: 8855818 doi: 10.1172/jci.insight.154573
Gundersen, H. et al. The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96, 857–881 (1988).
pubmed: 3056461 doi: 10.1111/j.1699-0463.1988.tb00954.x
Fehrenbach, A. et al. Stereological estimation of the volume weighted mean volumes of alveoli and acinar pathways in the rat lung to characterise alterations after ischaemia/reperfusion. J. Anat. 194(Pt 1), 127–135 (1999).
pubmed: 10227674 doi: 10.1046/j.1469-7580.1999.19410127.x
Knudsen, L., Weibel, E. R., Gundersen, H. J., Weinstein, F. V. & Ochs, M. Assessment of air space size characteristics by intercept (chord) measurement: An accurate and efficient stereological approach. J. Appl. Physiol. 2010(108), 412–421 (1985).
Sousa, M.L.A., Katira, B.H., Bouch, S., Hsing, V., Engelberts, D., Amato, M., Post, M., Brochard, L.J. Limiting overdistention or collapse when mechanically ventilating injured lungs: A randomized study in a porcine model. Am. J. Respir. Crit. Care Med. (2024).
Knudsen, L. & Ochs, M. The micromechanics of lung alveoli: Structure and function of surfactant and tissue components. Histochem. Cell Biol. 150, 661–676 (2018).
pubmed: 30390118 pmcid: 6267411 doi: 10.1007/s00418-018-1747-9
Knudsen, L. et al. Acinar micromechanics in health and lung injury: What we have learned from quantitative morphology. Front. Physiol. 14, 1142221 (2023).
pubmed: 37025383 pmcid: 10070844 doi: 10.3389/fphys.2023.1142221
Knudsen, L. et al. Alveolar micromechanics in bleomycin-induced lung injury. Am. J. Respir. Cell Mol. Biol. 59, 757–769 (2018).
pubmed: 30095988 pmcid: 6293074 doi: 10.1165/rcmb.2018-0044OC
Wallbank, A. M. et al. CNP-miR146a improves outcomes in a two-hit acute- and ventilator-induced lung injury model. Nanomedicine 50, 102679 (2023).
pubmed: 37116556 doi: 10.1016/j.nano.2023.102679
Albert, R. K., Smith, B., Perlman, C. E. & Schwartz, D. A. Is progression of pulmonary fibrosis due to ventilation-induced lung injury?. Am. J. Respir. Crit. Care Med. 200, 140–151 (2019).
pubmed: 31022350 pmcid: 6635778 doi: 10.1164/rccm.201903-0497PP
Roan, E. & Waters, C. M. What do we know about mechanical strain in lung alveoli?. Am. J. Physiol. Lung Cell Mol. Physiol. 301, L625-635 (2011).
pubmed: 21873445 pmcid: 3213982 doi: 10.1152/ajplung.00105.2011
Jimenez, J. V. et al. Electric impedance tomography-guided PEEP titration reduces mechanical power in ARDS: A randomized crossover pilot trial. Crit. Care 27, 21 (2023).
pubmed: 36650593 pmcid: 9843117 doi: 10.1186/s13054-023-04315-x
Liu, X. et al. Electrical impedance tomography for titration of positive end-expiratory pressure in acute respiratory distress syndrome patients with chronic obstructive pulmonary disease. Crit. Care 26, 339 (2022).
pubmed: 36333809 pmcid: 9635124 doi: 10.1186/s13054-022-04201-y
Bachmann, M. C. et al. Electrical impedance tomography in acute respiratory distress syndrome. Crit. Care 22, 263 (2018).
pubmed: 30360753 pmcid: 6203288 doi: 10.1186/s13054-018-2195-6
Rühl, N. et al. Surfactant protein B deficiency induced high surface tension: relationship between alveolar micromechanics, alveolar fluid properties and alveolar epithelial cell injury. Int. J. Mol. Sci. 20, 4243 (2019).
pubmed: 31480246 pmcid: 6747270 doi: 10.3390/ijms20174243
Hantos, Z., Collins, R. A., Turner, D. J., Jánosi, T. Z. & Sly, P. D. Tracking of airway and tissue mechanics during TLC maneuvers in mice. J. Appl. Physiol. 2003(95), 1695–1705 (1985).

Auteurs

Franziska Roeder (F)

Institute of Functional and Applied Anatomy, Hannover Medical School, Hannover, Germany.

Tina Röpke (T)

Department of Experimental Pneumology, Hannover Medical School, Hannover, Germany.

Lara-Kristin Steinmetz (LK)

Department of Experimental Pneumology, Hannover Medical School, Hannover, Germany.

Martin Kolb (M)

Department of Medicine, Firestone Institute for Respiratory Health, McMaster University, Hamilton, ON, Canada.

Ulrich A Maus (UA)

Department of Experimental Pneumology, Hannover Medical School, Hannover, Germany.
Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of the German Center for Lung Disease (DZL), Hannover, Germany.

Bradford J Smith (BJ)

Department of Bioengineering, College of Engineering Design and Computing, University of Colorado Denver|Anschutz Medical Campus, Aurora, CO, USA.
Department of Pediatric Pulmonary and Sleep Medicine, School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO, USA.

Lars Knudsen (L)

Institute of Functional and Applied Anatomy, Hannover Medical School, Hannover, Germany. Knudsen.lars@mh-hannover.de.
Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of the German Center for Lung Disease (DZL), Hannover, Germany. Knudsen.lars@mh-hannover.de.

Classifications MeSH