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Analysis of pediatric airway morphology using statistical shape modeling

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An Erratum to this article was published on 27 January 2016

Abstract

Traditional studies of airway morphology typically focus on individual measurements or relatively simple lumped summary statistics. The purpose of this work was to use statistical shape modeling (SSM) to synthesize a skeleton model of the large bronchi of the pediatric airway tree and to test for overall airway shape differences between two populations. Airway tree anatomy was segmented from volumetric chest computed tomography of 20 control subjects and 20 subjects with cystic fibrosis (CF). Airway centerlines, particularly bifurcation points, provide landmarks for SSM. Multivariate linear and logistic regression was used to examine the relationships between airway shape variation, subject size, and disease state. Leave-one-out cross-validation was performed to test the ability to detect shape differences between control and CF groups. Simulation experiments, using tree shapes with known size and shape variations, were performed as a technical validation. Models were successfully created using SSM methods. Simulations demonstrated that the analysis process can detect shape differences between groups. In clinical data, CF status was discriminated with good accuracy (precision = 0.7, recall = 0.7) in leave-one-out cross-validation. Logistic regression modeling using all subjects showed a good fit (ROC AUC = 0.85) and revealed significant differences in SSM parameters between control and CF groups. The largest mode of shape variation was highly correlated with subject size (R = 0.95, p < 0.001). SSM methodology can be applied to identify shape differences in the airway between two populations. This method suggests that subtle shape differences exist between the CF airway and disease control.

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References

  1. Agresti A (2007) An introduction to categorical data analysis. Wiley-Interscience, New York

    Book  Google Scholar 

  2. Ardekani S, Weiss RG, Lardo AC, George RT, Lima JA, Wu KC, Miller MI, Winslow RL, Younes L (2009) Computational method for identifying and quantifying shape features of human left ventricular remodeling. Ann Biomed Eng 37:1043–1054. doi:10.1007/s10439-009-9677-2

    Article  PubMed  PubMed Central  Google Scholar 

  3. Aysola RS, Hoffman EA, Gierada D, Wenzel S, Cook-Granroth J, Tarsi J, Zheng J, Schechtman KB, Ramkumar TP, Cochran R et al (2008) Airway remodeling measured by multidetector CT is increased in severe asthma and correlates with pathology. Chest 134:1183–1191. doi:10.1378/chest.07-2779

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chan HF, Clark AR, Hoffman EA, Malcolm DT, Tawhai MH (2015) Quantifying normal geometric variation in human pulmonary lobar geometry from high resolution computed tomography. J Biomech Eng 137:051010. doi:10.1115/1.4029919

    Article  PubMed  Google Scholar 

  5. Cootes TF, Edwards G, Taylor CJ (2001) Active appearance models. IEEE Trans Pattern Anal Mach Intell 23:681–685

    Article  Google Scholar 

  6. Cootes TF, Taylor CJ, Cooper DH, Graham J (1995) Active shape models: their training and application. Comput Vis Image Underst 61:38–59

    Article  Google Scholar 

  7. Coxson HO (2008) Quantitative computed tomography assessment of airway wall dimensions: current status and potential applications for phenotyping chronic obstructive pulmonary disease. Proc Am Thoracic Soc 5:940–945. doi:10.1513/pats.200806-057QC

    Article  Google Scholar 

  8. Davies RH, Twining CJ, Cootes TF, Taylor CJ (2010) Building 3-D statistical shape models by direct optimization. IEEE Trans Med Imaging 29:961–981. doi:10.1109/TMI.2009.2035048

    Article  PubMed  Google Scholar 

  9. de Jong PA, Long FR, Wong JC, Merkus PJ, Tiddens HA, Hogg JC, Coxson HO (2006) Computed tomographic estimation of lung dimensions throughout the growth period. Eur Respir J 27:261–267. doi:10.1183/09031936.06.00070805

    Article  PubMed  Google Scholar 

  10. de Jong PA, Nakano Y, Hop WC, Long FR, Coxson HO, Pare PD, Tiddens HA (2005) Changes in airway dimensions on computed tomography scans of children with cystic fibrosis. Am J Respir Crit Care Med 172:218–224. doi:10.1164/rccm.200410-1311OC

    Article  PubMed  Google Scholar 

  11. DeBoer EM, Swiercz W, Heltshe SL, Anthony MM, Szefler P, Klein R, Strain J, Brody AS, Sagel SD (2014) Automated CT scan scores of bronchiectasis and air trapping in cystic fibrosis. Chest 145:593–603. doi:10.1378/chest.13-0588

    Article  PubMed  PubMed Central  Google Scholar 

  12. Du Bois D, Du Bois EF (1916) Clinical calorimetry: tenth paper a formula to estimate the approximate surface area if height and weight be known. Arch Intern Med 17(6):863–871

    Article  Google Scholar 

  13. FitzSimmons SC (1993) The changing epidemiology of cystic fibrosis. J Pediatr 122:1–9

    Article  CAS  PubMed  Google Scholar 

  14. Gutierrez-Becker B, Arambula Cosio F, Guzman Huerta ME, Benavides-Serralde JA, Camargo-Marin L, Medina Banuelos V (2013) Automatic segmentation of the fetal cerebellum on ultrasound volumes, using a 3D statistical shape model. Med Biol Eng Comput 51:1021–1030. doi:10.1007/s11517-013-1082-1

    Article  PubMed  Google Scholar 

  15. Hafner BJ, Zachariah SG, Sanders JE (2000) Characterisation of three-dimensional anatomic shapes using principal components: application to the proximal tibia. Med Biol Eng Comput 38:9–16

    Article  CAS  PubMed  Google Scholar 

  16. Hastie T, Tibshirani R, Friedman JH (2009) The elements of statistical learning: data mining, inference, and prediction, 2nd edn. Springer, New York

    Book  Google Scholar 

  17. Heimann T, Meinzer HP (2009) Statistical shape models for 3D medical image segmentation: a review. Med Image Anal 13:543–563. doi:10.1016/j.media.2009.05.004

    Article  PubMed  Google Scholar 

  18. Horsfield K (1990) Diameters, generations, and orders of branches in the bronchial tree. J Appl Physiol 68:457–461

    CAS  PubMed  Google Scholar 

  19. Kendall DG (1977) The diffusion of shape. Adv In Appl Prob 9:428–430

    Article  Google Scholar 

  20. Kitaoka H, Takaki R, Suki B (1999) A three-dimensional model of the human airway tree. J Appl Physiol 87:2207–2217

    CAS  PubMed  Google Scholar 

  21. Leonardi B, Taylor AM, Mansi T, Voigt I, Sermesant M, Pennec X, Ayache N, Boudjemline Y, Pongiglione G (2013) Computational modelling of the right ventricle in repaired tetralogy of Fallot: can it provide insight into patient treatment? Eur Heart J Cardiovasc Imaging 14:381–386. doi:10.1093/ehjci/jes239

    Article  PubMed  PubMed Central  Google Scholar 

  22. Long FR, Williams RS, Castile RG (2004) Structural airway abnormalities in infants and young children with cystic fibrosis. J Pediatr 144:154–161. doi:10.1016/j.jpeds.2003.09.026

    Article  PubMed  Google Scholar 

  23. Lordkipanidze D, Ponce de Leon MS, Margvelashvili A, Rak Y, Rightmire GP, Vekua A, Zollikofer CP (2013) A complete skull from Dmanisi, Georgia, and the evolutionary biology of early Homo. Science 342:326–331. doi:10.1126/science.1238484

    Article  CAS  PubMed  Google Scholar 

  24. Mauroy B, Fausser C, Pelca D, Merckx J, Flaud P (2011) Toward the modeling of mucus draining from the human lung: role of the geometry of the airway tree. Phys Biol 8:056006. doi:10.1088/1478-3975/8/5/056006

    Article  PubMed  Google Scholar 

  25. Mauroy B, Filoche M, Andrade JS Jr, Sapoval B (2003) Interplay between geometry and flow distribution in an airway tree. Phys Rev Lett 90:148101

    Article  CAS  PubMed  Google Scholar 

  26. Meyerholz DK, Stoltz DA, Namati E, Ramachandran S, Pezzulo AA, Smith AR, Rector MV, Suter MJ, Kao S, McLennan G et al (2010) Loss of cystic fibrosis transmembrane conductance regulator function produces abnormalities in tracheal development in neonatal pigs and young children. Am J Respir Crit Care Med 182:1251–1261. doi:10.1164/rccm.201004-0643OC

    Article  PubMed  PubMed Central  Google Scholar 

  27. Montaudon M, Berger P, Cangini-Sacher A, de Dietrich G, Tunon-de-Lara JM, Marthan R, Laurent F (2007) Bronchial measurement with three-dimensional quantitative thin-section CT in patients with cystic fibrosis. Radiology 242:573–581. doi:10.1148/radiol.2422060030

    Article  PubMed  Google Scholar 

  28. Mott LS, Park J, Murray CP, Gangell CL, de Klerk NH, Robinson PJ, Robertson CF, Ranganathan SC, Sly PD, Stick SM (2012) Progression of early structural lung disease in young children with cystic fibrosis assessed using CT. Thorax 67:509–516. doi:10.1136/thoraxjnl-2011-200912

    Article  PubMed  Google Scholar 

  29. Rao L, Tiller C, Coates C, Kimmel R, Applegate KE, Granroth-Cook J, Denski C, Nguyen J, Yu Z, Hoffman E et al (2010) Lung growth in infants and toddlers assessed by multi-slice computed tomography. Acad Radiol 17:1128–1135. doi:10.1016/j.acra.2010.04.012

    Article  PubMed  PubMed Central  Google Scholar 

  30. Refojo MF (1982) Molecular shape and effective diffusion radius. Invest Ophthalmol Vis Sci 22:129–130

    CAS  PubMed  Google Scholar 

  31. Sarria EE, Mattiello R, Rao L, Tiller CJ, Poindexter B, Applegate KE, Granroth-Cook J, Denski C, Nguyen J, Yu Z et al (2011) Quantitative assessment of chronic lung disease of infancy using computed tomography. Eur Respir J 39:992–999. doi:10.1183/09031936.00064811

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sly PD, Brennan S, Gangell C, de Klerk N, Murray C, Mott L, Stick SM, Robinson PJ, Robertson CF, Ranganathan SC (2009) Lung disease at diagnosis in infants with cystic fibrosis detected by newborn screening. Am J Respir Crit Care Med 180:146–152. doi:10.1164/rccm.200901-0069OC

    Article  PubMed  Google Scholar 

  33. Tschirren J, Hoffman EA, McLennan G, Sonka M (2005) Intrathoracic airway trees: segmentation and airway morphology analysis from low-dose CT scans. IEEE Trans Med Imaging 24:1529–1539. doi:10.1109/TMI.2005.857654

    Article  PubMed  PubMed Central  Google Scholar 

  34. Vaillant M, Glaunes J (2005) Surface matching via currents. Inf Proc Med Imaging Proc Conf 19:381–392

    Google Scholar 

  35. Weibel ER (2013) It takes more than cells to make a good lung. Am J Respir Crit Care Med 187:342–346. doi:10.1164/rccm.201212-2260OE

    Article  CAS  PubMed  Google Scholar 

  36. Wielputz MO, Eichinger M, Weinheimer O, Ley S, Mall MA, Wiebel M, Bischoff A, Kauczor HU, Heussel CP, Puderbach M (2013) Automatic airway analysis on multidetector computed tomography in cystic fibrosis: correlation with pulmonary function testing. J Thorac Imaging 28:104–113. doi:10.1097/RTI.0b013e3182765785

    Article  PubMed  Google Scholar 

  37. Williamson JP, James AL, Phillips MJ, Sampson DD, Hillman DR, Eastwood PR (2009) Quantifying tracheobronchial tree dimensions: methods, limitations and emerging techniques. Eur Respir J 34:42–55. doi:10.1183/09031936.00020408

    Article  CAS  PubMed  Google Scholar 

  38. Zelditch M (2004) Geometric morphometrics for biologists: a primer. Elsevier, Amsterdam

    Google Scholar 

Download references

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Correspondence to Stephen M. Humphries.

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Humphries, S.M., Hunter, K.S., Shandas, R. et al. Analysis of pediatric airway morphology using statistical shape modeling. Med Biol Eng Comput 54, 899–911 (2016). https://doi.org/10.1007/s11517-015-1445-x

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  • DOI: https://doi.org/10.1007/s11517-015-1445-x

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