Abstract
Tracheobronchial stents are used to restore patency to stenosed airways. However, these devices are associated with many complications such as stent migration, granulation tissue formation, mucous plugging and stent strut fracture. Of these, granulation tissue formation is the complication that most frequently requires costly secondary interventions. In this study a biomechanical lung modelling framework recently developed by the authors to capture the lung in-vivo stress state under physiological loading is employed in conjunction with ovine pre-clinical stenting results and device experimental data to evaluate the effect of stent interaction on granulation tissue formation. Stenting is simulated using a validated model of a prototype covered laser-cut tracheobronchial stent in a semi-specific biomechanical lung model, and physiological loading is performed. Two computational methods are then used to predict possible granulation tissue formation: the standard method which utilises the increase in maximum principal stress change, and a newly proposed method which compares the change in contact pressure over a respiratory cycle. These computational predictions of granulation tissue formation are then compared to pre-clinical stenting observations after a 6-week implantation period. Experimental results of the pre-clinical stent implantation showed signs of granulation tissue formation both proximally and distally, with a greater proximal reaction. The standard method failed to show a correlation with the experimental results. However, the contact change method showed an apparent correlation with granulation tissue formation. These results suggest that this new method could be used as a tool to improve future device designs.
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References
Al-Mayah A, Moseley J, Velec M et al (2010) Deformable image registration of heterogeneous human lung incorporating the bronchial tree. Med Phys 37:4560–4571. https://doi.org/10.1118/1.3471020
Al-Mayah A, Moseley J, Velec M, Brock K (2011) Toward efficient biomechanical-based deformable image registration of lungs for image-guided radiotherapy. Phys Med Biol 56:4701–13. https://doi.org/10.1088/0031-9155/56/15/005
Auricchio F, Taylor R, Lubliner J (1997) Shape-memory alloys: macromodelling and numerical simulations of the superelastic behavior. Comput methods Appl 146(3):281–312
Bähr A, Wolf E (2012) Domestic animal models for biomedical research. Reprod Domest Anim 47:59–71. https://doi.org/10.1111/j.1439-0531.2012.02056.x
Bols J, Degroote J, Trachet B et al (2013) A computational method to assess the in vivo stresses and unloaded configuration of patient-specific blood vessels. J Comput Appl Math 246:10–17. https://doi.org/10.1016/j.cam.2012.10.034
Brock KK (2010) Results of a Multi-Institution Deformable Registration Accuracy Study (MIDRAS). Int J Radiat Oncol Biol Phys 76:583–596. https://doi.org/10.1016/j.ijrobp.2009.06.031
Burningham AR, Wax MK, Andersen PE et al (2002) Metallic tracheal stents: complications associated with long-term use in the upper airway. Ann Otol Rhinol Laryngol 111:285–90
Chaure J, Serrano C, Fernández-Parra R et al (2016) On studying the interaction between different stent models and rabbit tracheal tissue: numerical, endoscopic and histological comparison. Ann Biomed Eng 44:368–381. https://doi.org/10.1007/s10439-015-1504-3
Chen W, Clauser J, Thiebes AL et al (2016) Selection and fabrication of a non-woven polycarbonate urethane cover for a tissue engineered airway stent. Int J Pharm 514:255–262. https://doi.org/10.1016/j.ijpharm.2016.06.047
Chung FT, Lin SM, Chen HC et al (2008) Factors leading to tracheobronchial self-expandable metallic stent fracture. J Thorac Cardiovasc Surg 136:1328–1335. https://doi.org/10.1016/j.jtcvs.2008.05.039
Chung F-T, Chen H-C, Chou C-L et al (2011) An outcome analysis of self-expandable metallic stents in central airway obstruction: a cohort study. J Cardiothorac Surg 6:46. https://doi.org/10.1186/1749-8090-6-46
Codd SL, Lambert RK, Alley MR, Pack RJ (1994) Tensile stiffness of ovine tracheal wall. J Appl Physiol 76:2627–2635
Conway C, Sharif F, McGarry JP, McHugh PE (2012) A computational test-bed to assess coronary stent implantation mechanics using a population-specific approach. Cardiovasc Eng Technol 3:374–387. https://doi.org/10.1007/s13239-012-0104-8
De Bock S, Iannaccone F, De Beule M et al (2013) Filling the void: a coalescent numerical and experimental technique to determine aortic stent graft mechanics. J Biomech 46:2477–82. https://doi.org/10.1016/j.jbiomech.2013.07.010
Dooms C, De Keukeleire T, Janssens A, Carron K (2009) Performance of fully covered self-expanding metallic stents in benign airway strictures. Respiration 77:420–6. https://doi.org/10.1159/000203364
Ehrhardt J, Werner R, Schmidt-Richberg A et al (2008) Generation of a mean motion model of the lung using 4D-CT Image Data. Eurographics Workshop Vis Comput Biomed. https://doi.org/10.2312/VCBM/VCBM08/069-076
Ehrhardt J, Werner R, Schmidt-Richberg A, Handels H (2011) Statistical modeling of 4D respiratory lung motion using diffeomorphic image registration. IEEE Trans Med Imaging 30:251–265. https://doi.org/10.1109/TMI.2010.2076299
Fernández-Bussy S, Majid A, Caviedes I et al (2011) Treatment of airway complications following lung transplantation. Arch Bronconeumol (English Ed) 47:128–133. https://doi.org/10.1016/S1579-2129(11)70031-3
Freitag L (2010) Airway stents. In: Strausz J, Bolliger CT (eds) Interventional pulmonology. European Respiratory Society Journals Ltd, Sheffield, pp 190–217
Fuerst B, Mansi T, Carnis F et al (2015) Patient-specific biomechanical model for the prediction of lung motion from 4-D CT images. IEEE Trans Med Imaging 34:599–607. https://doi.org/10.1109/TMI.2014.2363611
García A, Peña E, Martínez MA (2012) Influence of geometrical parameters on radial force during self-expanding stent deployment. Application for a variable radial stiffness stent. J Mech Behav Biomed Mater 10:166–75. https://doi.org/10.1016/j.jmbbm.2012.02.006
Ghriallais RN, Bruzzi M (2014) Self-expanding stent modelling and radial force accuracy. Comput Methods Biomech Biomed Eng 17:318–333. https://doi.org/10.1080/10255842.2012.683427
Godoy MCB, Saldana DA, Rao PP et al (2014) Multidetector CT evaluation of airway stents: what the radiolo-gist should know. Radiographics 34:1793–1806. https://doi.org/10.1148/rg.347130063
Grewe PH, Müller KM, Lindstaedt M et al (2005) Reaction patterns of the tracheobronchial wall to implanted noncovered metal stents. Chest 128:986–990. https://doi.org/10.1378/chest.128.2.986
Grogan JA, Leen SB, McHugh PE (2013) Optimizing the design of a bioabsorbable metal stent using computer simulation methods. Biomaterials 34:8049–8060. https://doi.org/10.1016/j.biomaterials.2013.07.010
Guibert N, Mazieres J, Marquette CH et al (2015) Integration of interventional bronchoscopy in the management of lung cancer. Eur Respir Rev 24:378–391. https://doi.org/10.1183/16000617.00010014
Hautmann H, Rieger J, Huber RM, Pfeifer KJ (1999) Elastic deformation properties of implanted endobronchial wire stents in benign and malignant bronchial disease: a radiographic in vivo evaluation. Cardiovasc Intervent Radiol 22:103–8
Hu H-C, Liu Y-H, Wu Y-C et al (2011) Granulation tissue formation following Dumon airway stenting: the influence of stent diameter. Thorac Cardiovasc Surg 59:163–168
Hurewitz AN, Sidhu U, Bergofsky EH, Chanana AD (1984) How alterations in pleural pressure influence esophageal pressure. J Appl Physiol 56:1162–1169
Jeong BH, Um SW, Suh GY et al (2012) Results of interventional bronchoscopy in the management of postoperative tracheobronchial stenosis. J Thorac Cardiovasc Surg 144:217–222. https://doi.org/10.1016/j.jtcvs.2012.03.077
Lee P, Kupeli E, Mehta AC (2010) Airway stents. Clin Chest Med 31:141–150. https://doi.org/10.1016/j.ccm.2009.08.002
Lemaire A, Burfeind WR, Toloza E et al (2005) Outcomes of tracheobronchial stents in patients with malignant airway disease. Ann Thorac Surg 80:434–438. https://doi.org/10.1016/j.athoracsur.2005.02.071
Malvè M, Serrano C, Peña E et al (2014) Modelling the air mass transfer in a healthy and a stented rabbit trachea: CT-images, computer simulations and experimental study. Int Commun Heat Mass Transf 53:1–8. https://doi.org/10.1016/j.icheatmasstransfer.2014.02.001
Malvè M, Palomar Del AP, Chandra S et al (2011a) FSI analysis of a human trachea before and after prosthesis implantation. J Biomech Eng 133:71003. https://doi.org/10.1115/1.4004315
Malvè M, Pérez del Palomar a, Chandra S et al (2011b) FSI Analysis of a healthy and a stenotic human trachea under impedance-based boundary conditions. J Biomech Eng 133:21001. https://doi.org/10.1115/1.4003130
McGrath DJ, O’Brien B, Bruzzi M, McHugh PE (2014) Nitinol stent design-understanding axial buckling. J Mech Behav Biomed Mater 40:252–263. https://doi.org/10.1016/j.jmbbm.2014.08.029
McGrath DJ, O’Brien B, Bruzzi M et al (2016) Evaluation of cover effects on bare stent mechanical response. J Mech Behav Biomed Mater 61:567–580. https://doi.org/10.1016/j.jmbbm.2016.04.023
McGrath DJ, Thiebes AL, Cornelissen CG et al (2017) An ovine in vivo framework for tracheobronchial stent analysis. Biomech Model Mechanobiol. https://doi.org/10.1007/s10237-017-0904-8
Murphy K, van Ginneken B, Reinhardt JM et al (2011) Evaluation of registration methods on thoracic CT: the EMPIRE10 challenge. IEEE Trans Med Imaging 30:1901–1920. https://doi.org/10.1109/TMI.2011.2158349
Murthy SC, Gildea TR, Mehta AC (2004) Removal of self-expandable metallic stents: Is it possible? Semin Respir Crit Care Med 25:381–385. https://doi.org/10.1055/s-2004-832711
Nadzeyka I, Gabler C, Erarslan D et al (2014) Manufacturing of biocompatible nonwoven structures by using spray atomization of dissolved polymers. Polym Eng Sci 54:867–873. https://doi.org/10.1002/pen.23622
Noppen M, Stratakos G, D’Haese J et al (2005) Removal of covered self-expandable metallic airway stents in benign disorders: indications, technique, and outcomes. Chest 127:482–7. https://doi.org/10.1378/chest.127.2.482
Ost DE, Shah AM, Lei X et al (2012) Respiratory infections increase the risk of granulation tissue formation following airway stenting in patients with malignant airway obstruction. Chest 141:1473–81. https://doi.org/10.1378/chest.11-2005
Perez del Palomar A, Trabelsi O, Mena A et al (2010) Patient-specific models of human trachea to predict mechanical consequences of endoprosthesis implantation. Philos Trans R Soc A Math Phys Eng Sci 368:2881–2896. https://doi.org/10.1098/rsta.2010.0092
Puma F, Farabi R, Urbani M et al (2000) Long-term safety and tolerance of silicone and self-expandable airway stents: an experimental study. Ann Thorac Surg 69:1030–4
Rausch SMK, Martin C, Bornemann PB et al (2011) Material model of lung parenchyma based on living precision-cut lung slice testing. J Mech Behav Biomed Mater 4:583–92. https://doi.org/10.1016/j.jmbbm.2011.01.006
Razi SS, Lebovics RS, Schwartz G et al (2010) Timely airway stenting improves survival in patients with malignant central airway obstruction. Ann Thorac Surg 90:1088–1093. https://doi.org/10.1016/j.athoracsur.2010.06.093
Saad CP, Murthy S, Krizmanich G, Mehta AC (2003) Self-expandable metallic airway stents and flexible bronchoscopy. Chest 124:1993–1999. https://doi.org/10.1378/chest.124.5.1993
Saito Y, Imamura H (2005) Airway stenting. Surg Today 35:265–70. https://doi.org/10.1007/s00595-004-2942-y
Scheerlinck JPY, Snibson KJ, Bowles VM, Sutton P (2008) Biomedical applications of sheep models: from asthma to vaccines. Trends Biotechnol 26:259–266. https://doi.org/10.1016/j.tibtech.2008.02.002
Schmäl F, Fegeler W, Terpe HJ et al (2003) Bacteria and granulation tissue associated with Montgomery T-tubes. Laryngoscope 113:1394–1400. https://doi.org/10.1097/00005537-200308000-00024
Sheikhy H, Shahidzadeh M, Ramezanzadeh B, Noroozi F (2013) Studying the effects of chain extenders chemical structures on the adhesion and mechanical properties of a polyurethane adhesive. J Ind Eng Chem 19:1949–1955. https://doi.org/10.1016/j.jiec.2013.03.008
Si H, Gärtner K (2015) Meshing piecewise linear complexes by constrained delaunay tetrahedralizations. In: Proceedings of the 14th international meshing roundtable. Springer, Berlin, pp 147–163
Stoeckel D, Pelton A, Duerig T (2004) Self-expanding nitinol stents: material and design considerations. Eur Radiol 14:292–301. https://doi.org/10.1007/s00330-003-2022-5
Tawhai MH, Nash MP, Lin C-L, Hoffman E (2009) Supine and prone differences in regional lung density and pleural pressure gradients in the human lung with constant shape. J Appl Physiol 107:912–20. https://doi.org/10.1152/japplphysiol.00324.2009
Tehrani JN, Yang Y, Werner R et al (2015) Sensitivity of tumor motion simulation accuracy to lung biomechanical modeling approaches and parameters. Phys Med Biol 60:8833–8849. https://doi.org/10.1088/0031-9155/60/22/8833
Thiebes AL, Kelly N, Sweeney CA et al (2017) Pulmostent: in vitro to in vivo evaluation of a tissue engineered endobronchial stent. Ann Biomed Eng 45:873–883. https://doi.org/10.1007/s10439-016-1737-9
Trabelsi O, del Palomar AP, López-villalobos JL (2010) Experimental characterization and constitutive modeling of the mechanical behavior of the human trachea. Med Eng Phys 32:76–82. https://doi.org/10.1016/j.medengphy.2009.10.010
Trabelsi O, Pérez del Palomar A, Mena Tobar A et al (2011) FE simulation of human trachea swallowing movement before and after the implantation of an endoprothesis. Appl Math Model 35:4902–4912. https://doi.org/10.1016/j.apm.2011.03.041
Trabelsi O, Malve M, Mena Tobar A, Doblare M (2015) Simulation of swallowing dysfunction and mechanical ventilation after a Montgomery T-tube insertion. Comput Methods Biomech Biomed Eng 18:1596–1605. https://doi.org/10.1080/10255842.2014.930448
Villard P-F, Beuve M, Shariat B et al (2005) Simulation of lung behaviour with finite elements: influence of bio-mechanical parameters. In: Third international conference on medical information visualisation–biomedical visualisation. IEEE, pp 9–14
Wall WA, Rabczuk T (2008) Fluid-structure interaction in lower airways of CT-based lung geometries. Int J Numer Methods Fluids 57:653–675. https://doi.org/10.1002/fld.1763
Werner R, Ehrhardt J, Schmidt R, Handels H (2009) Patient-specific finite element modeling of respiratory lung motion using 4D CT image data. Med Phys 36:1500. https://doi.org/10.1118/1.3101820
West JB (2012) Respiratory physiology: the essentials. Lippincott Williams and Wilkins, Philadelphia
Zakaluzny SA, Lane JD, Mair EA (2003) Complications of tracheobronchial airway stents. Otolaryngol Head Neck Surg 128:478–88. https://doi.org/10.1016/mhn.2003.107
Acknowledgements
The research leading to these results has received funding from the European Union’s Seventh Framework Programme (FP7/2007-2013 under Grant Agreement No. NMP3-SL-2012-280915)-PulmoStent. Funding from the College of Engineering and Informatics at NUI Galway through a College Scholarship is also acknowledged, along with funding support provided by the Structured PhD Programme in Biomedical Engineering and Regenerative Medicine (BMERM). Funded under the Programme for Research in Third-Level Institutions (PRTLI) Cycle 5 (Strand 2) and co-funded under the European Regional Development Fund (ERDF). The authors wish to acknowledge the SFI/HEA Irish Centre for High-End Computing (ICHEC) for the provision of computational facilities and support.
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McGrath, D.J., Thiebes, A.L., Cornelissen, C.G. et al. Evaluating the interaction of a tracheobronchial stent in an ovine in-vivo model. Biomech Model Mechanobiol 17, 499–516 (2018). https://doi.org/10.1007/s10237-017-0974-7
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DOI: https://doi.org/10.1007/s10237-017-0974-7