Abstract
Robin Sequence (RS) is a potentially fatal craniofacial condition characterized by undersized jaw, posteriorly displaced tongue, and resultant upper airway obstruction (UAO). Accurate assessment of UAO severity is crucial for management and diagnosis of RS, yet current evaluation modalities have significant limitations and no quantitative measures of airway resistance exist. In this study, we combine 4-dimensional computed tomography and computational fluid dynamics (CFD) to assess, for the first time, UAO severity using fluid dynamic metrics in RS patients. Dramatic intrapopulation differences are found, with the ratio between most and least severe patients in breathing resistance, energy loss, and peak velocity equal to 40:1, 20:1, and 6:1, respectively. Analysis of local airflow dynamics characterized patients as presenting with primary obstructions either at the location of the tongue base, or at the larynx, with tongue base obstructions resulting in a more energetic stenotic jet and greater breathing resistance. Finally, CFD-derived flow metrics are found to correlate with the level of clinical respiratory support. Our results highlight the large intrapopulation variability, both in quantitative metrics of UAO severity (resistance, energy loss, velocity) and in the location and intensity of stenotic jets for RS patients. These results suggest that computed airflow metrics may significantly improve our understanding of UAO and its management in RS.
Similar content being viewed by others
References
Barker, A. J., P. van Ooij, K. Bandi, J. Garcia, M. Albaghdadi, P. McCarthy, R. O. Bonow, J. Carr, J. Collins, S. C. Malaisrie, and M. Markl. Viscous energy loss in the presence of abnormal aortic flow: energy loss in the presence of abnormal aortic flow. Magn. Reson. Med. 72:620–628, 2014.
Bates, A. J., A. Comerford, R. Cetto, R. C. Schroter, N. S. Tolley, and D. J. Doorly. Power loss mechanisms in pathological tracheas. J. Biomech. 49:2187–2192, 2016.
Bates, A. J., A. Schuh, G. Amine-Eddine, K. McConnell, W. Loew, R. J. Fleck, J. C. Woods, C. L. Dumoulin, and R. S. Amin. Assessing the relationship between movement and airflow in the upper airway using computational fluid dynamics with motion determined from magnetic resonance imaging. Clin. Biomech. 66:88–96, 2019.
Brouns, M., S. T. Jayaraju, C. Lacor, J. De Mey, M. Noppen, W. Vincken, and S. Verbanck. Tracheal stenosis: a flow dynamics study. J. Appl. Physiol. 102:1178–1184, 2007.
Chakkarapani, A. A., R. Adappa, S. K. Mohammad Ali, S. Gupta, N. B. Soni, L. Chicoine, and H. D. Hummler. Current concepts of mechanical ventilation in neonates—Part 1: Basics. Int. J. Pediatrics Adolesc. Med. 7:15–20, 2020.
Costa, M. A., M. M. Tu, K. P. Murage, S. S. Tholpady, W. A. Engle, and R. L. Flores. Robin sequence: mortality, causes of death, and clinical outcomes. Plast. Reconstruct. Surg. 134:738–745, 2014.
Donati, F., C. A. Figueroa, N. P. Smith, P. Lamata, and D. A. Nordsletten. Non-invasive pressure difference estimation from PC-MRI using the work-energy equation. Med. Image Anal. 26:159–172, 2015.
Evans, K. N., K. C. Sie, R. A. Hopper, R. P. Glass, A. V. Hing, and M. L. Cunningham. Robin sequence: from diagnosis to development of an effective management plan. Pediatrics. 127:936–948, 2011.
Faizal, W. M., N. N. N. Ghazali, C. Y. Khor, I. A. Badruddin, M. Z. Zainon, A. A. Yazid, N. B. Ibrahim, and R. M. Razi. Computational fluid dynamics modelling of human upper airway: a review. Comput. Methods Prog. Biomed. 196:105627, 2020.
Fayoux, P., S. J. Daniel, G. Allen, K. Balakrishnan, A. Boudewyns, A. Cheng, A. De Alarcon, D. Goel, C. K. Hart, N. Leboulanger, G. Lee, E. Moreddu, H. Muntz, R. Rahbar, R. Nicollas, C. R. Rogers-Vizena, J. Russell, M. J. Rutter, R. J. H. Smith, M. Wyatt, G. Zalzal, and C. M. Resnick. International Pediatric ORL Group (IPOG) Robin Sequence consensus recommendations. Int. J. Pediatric Otorhinolaryngol. 130:109855, 2020.
Green, A. S. Modelling of peak-flow wall shear stress in major airways of the lung. J. Biomech. 37:661–667, 2004.
Lam, A. S., M. D. Bindschadler, K. N. Evans, S. D. Friedman, M. S. Blessing, R. Bly, M. L. Cunningham, M. A. Egbert, R. E. Ettinger, E. R. Gallagher, R. A. Hopper, K. Johnson, J. A. Perkins, E. K. Romberg, K. C. Y. Sie, S. M. Susarla, C. J. Zdanski, X. Wang, J. P. Otjen, F. A. Perez, and J. P. Dahl. Accuracy and reliability of 4D-CT and flexible laryngoscopy in upper airway evaluation in robin sequence. Otolaryngol Head Neck Surg. 2021. https://doi.org/10.1177/01945998211027353.
Lam, A. S., M. D. Bindschadler, K. N. Evans, S. D. Friedman, J. P. Otjen, C. J. Zdanski, F. A. Perez, and J. P. Dahl. 4D computed tomography for dynamic upper airway evaluation in robin sequence. Otolaryngol Head Neck Surg. 165:905–908, 2021.
Lee, J. J., M. D. Ford, A. B. Tobey, and N. Jabbour. Diagnosing tongue base obstruction in pierre robin sequence infants: sleep vs awake endoscopy. Cleft Palate-Craniofacial J. 55:692–696, 2018.
Lee, V. S., K. N. Evans, F. A. Perez, A. P. Oron, and J. A. Perkins. Upper airway computed tomography measures and receipt of tracheotomy in infants with robin sequence. JAMA Otolaryngol Head Neck Surg. 142:750, 2016.
Lin, E. L., J. M. Bock, C. J. Zdanski, J. S. Kimbell, and G. J. M. Garcia. Relationship between degree of obstruction and airflow limitation in subglottic stenosis: CFD Study of Subglottic Stenosis. Laryngoscope. 128:1551–1557, 2018.
Mason, E. C., Z. Wu, S. McGhee, J. Markley, M. Koenigs, A. Onwuka, T. Chiang, and K. Zhao. Computational fluid dynamic modeling reveals nonlinear airway stress during trachea development. J. Pediatrics. 238:324-328.e1, 2021.
Mhlaba, J. M., M. L. Chen, H. P. Bandla, F. M. Baroody, and R. R. Reid. Predictive soft tissue airway volume analysis in mandibular distraction: pushing the envelope in surgical planning for obstructive sleep apnea. J. Craniofacial Surg. 27:181–184, 2016.
Moghaddam, MGh., G. J. M. Garcia, D. O. Frank-Ito, J. S. Kimbell, and J. S. Rhee. Virtual septoplasty: a method to predict surgical outcomes for patients with nasal airway obstruction. Int. J. CARS. 15:725–735, 2020.
Mylavarapu, G., M. Mihaescu, L. Fuchs, G. Papatziamos, and E. Gutmark. Planning human upper airway surgery using computational fluid dynamics. J. Biomech. 46:1979–1986, 2013.
Pedley, T. J. Pulmonary fluid dynamics. Annu. Rev. Fluid Mech. 9:229–274, 1977.
Pibarot, P., D. Garcia, and J. G. Dumesnil. Energy loss index in aortic stenosis: from fluid mechanics concept to clinical application. Circulation. 127:1101–1104, 2013.
Rhee, J. S. Role of virtual surgery in preoperative planning: assessing the individual components of functional nasal airway surgery. Arch. Facial Plast. Surg. 14:354, 2012.
Rios, G., R. J. Morrison, Y. Song, S. J. Fernando, C. Wootten, A. Gelbard, and H. Luo. Computational fluid dynamics analysis of surgical approaches to bilateral vocal fold immobility. Laryngoscope. 130:E57–E64, 2020.
Schwab, R. J., W. B. Gefter, E. A. Hoffman, K. B. Gupta, and A. I. Pack. Dynamic upper airway imaging during awake respiration in normal subjects and patients with sleep disordered breathing. Am. Rev. Respir. Dis. 148:1385–1400, 1993.
Sul, B., Z. Oppito, S. Jayasekera, B. Vanger, A. Zeller, M. Morris, K. Ruppert, T. Altes, V. Rakesh, S. Day, R. Robinson, J. Reifman, and A. Wallqvist. Assessing airflow sensitivity to healthy and diseased lung conditions in a computational fluid dynamics model validated in vitro. J. Biomech. Eng. 140:051009, 2018.
White, F. M. Fluid Mechanics. New York: McGraw-Hill, p. 862, 2009.
Wootton, D. M., H. Luo, S. C. Persak, S. Sin, J. M. McDonough, C. R. Isasi, and R. Arens. Computational fluid dynamics endpoints to characterize obstructive sleep apnea syndrome in children. J. Appl. Physiol. 116:104–112, 2014.
Xiao, Q., R. Cetto, D. J. Doorly, A. J. Bates, J. N. Rose, C. McIntyre, A. Comerford, G. Madani, N. S. Tolley, and R. Schroter. Assessing changes in airflow and energy loss in a progressive tracheal compression before and after surgical correction. Ann. Biomed. Eng. 48:822–833, 2020.
Xu, C., S. Sin, J. M. McDonough, J. K. Udupa, A. Guez, R. Arens, and D. M. Wootton. Computational fluid dynamics modeling of the upper airway of children with obstructive sleep apnea syndrome in steady flow. J. Biomech. 39:2043–2054, 2006.
Xu, X., J. Wu, W. Weng, and M. Fu. Investigation of inhalation and exhalation flow pattern in a realistic human upper airway model by PIV experiments and CFD simulations. Biomech. Model Mechanobiol. 19:1679–1695, 2020.
Zhu, L., X. Gong, J. Liu, Y. Li, Y. Zhong, J. Shen, and Z. Xu. Computational evaluation of surgical design for multisegmental complex congenital tracheal stenosis. BioMed Res. Int. 1–10:2020, 2020.
Acknowledgments
This research was supported by a National Institute of Health T-32 training Grant (NIH 5T32DC000018-38).
Conflict of interest
No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Stefan M. Duma oversaw the review of this article.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary file1 (MP4 2278 kb)
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Barbour, M., Richardson, C., Bindschadler, M. et al. Analysis of Upper Airway Flow Dynamics in Robin Sequence Infants Using 4-D Computed Tomography and Computational Fluid Dynamics. Ann Biomed Eng 51, 363–376 (2023). https://doi.org/10.1007/s10439-022-03036-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-022-03036-6