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Inter-operator Reliability of Magnetic Resonance Image-Based Computational Fluid Dynamics Prediction of Cerebrospinal Fluid Motion in the Cervical Spine

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Abstract

For the first time, inter-operator dependence of MRI based computational fluid dynamics (CFD) modeling of cerebrospinal fluid (CSF) in the cervical spinal subarachnoid space (SSS) is evaluated. In vivo MRI flow measurements and anatomy MRI images were obtained at the cervico-medullary junction of a healthy subject and a Chiari I malformation patient. 3D anatomies of the SSS were reconstructed by manual segmentation by four independent operators for both cases. CFD results were compared at nine axial locations along the SSS in terms of hydrodynamic and geometric parameters. Intraclass correlation (ICC) assessed the inter-operator agreement for each parameter over the axial locations and coefficient of variance (CV) compared the percentage of variance for each parameter between the operators. Greater operator dependence was found for the patient (0.19 < ICC < 0.99) near the craniovertebral junction compared to the healthy subject (ICC > 0.78). For the healthy subject, hydraulic diameter and Womersley number had the least variance (CV = ~2%). For the patient, peak diastolic velocity and Reynolds number had the smallest variance (CV = ~3%). These results show a high degree of inter-operator reliability for MRI-based CFD simulations of CSF flow in the cervical spine for healthy subjects and a lower degree of reliability for patients with Type I Chiari malformation.

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References

  1. Augst, A. D., D. C. Barratt, A. D. Hughes, F. P. Glor, S. A. M. Thom, and X. Y. Xu. Accuracy and reproducibility of CFD predicted wall shear stress using 3D ultrasound images. J. Biomech. Eng. 125(2):218–222, 2003.

    Article  CAS  PubMed  Google Scholar 

  2. Baledent, O., C. Gondry-Jouet, M. E. Meyer, G. De Marco, D. Le Gars, M. C. Henry-Feugeas, and I. Idy-Peretti. Relationship between cerebrospinal fluid and blood dynamics in healthy volunteers and patients with communicating hydrocephalus. Invest. Radiol. 39(1):45–55, 2004.

    Article  PubMed  Google Scholar 

  3. Baledent, O., M. C. Henry-Feugeas, and I. Idy-Peretti. Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest. Radiol. 36(7):368–377, 2001.

    Article  CAS  PubMed  Google Scholar 

  4. Bertram, C. D. Evaluation by fluid/structure-interaction spinal-cord simulation of the effects of subarachnoid-space stenosis on an adjacent syrinx. J. Biomech. Eng. 132(6):061009, 2010. doi:10.1115/1.4001165.

    Article  CAS  PubMed  Google Scholar 

  5. Bertram, C. D., A. R. Brodbelt, and M. A. Stoodley. The origins of syringomyelia: numerical models of fluid/structure interactions in the spinal cord. J. Biomech. Eng. 127(7):1099–1109, 2005.

    Article  CAS  PubMed  Google Scholar 

  6. Bruni, J. E. Cerebral ventricular system and cerebrospinal fluid encyclopedia of human biology. 1977.

  7. Bunck, A. C., J. R. Kroeger, A. Juettner, A. Brentrup, B. Fiedler, G. R. Crelier, B. A. Martin, W. Heindel, D. Maintz, W. Schwindt, et al. Magnetic resonance 4D flow analysis of cerebrospinal fluid dynamics in Chiari I malformation with and without syringomyelia. Eur. Radiol. 22(9):1860–1870, 2012.

    Article  PubMed  Google Scholar 

  8. Bunck, A. C., J. R. Kroger, A. Juttner, A. Brentrup, B. Fiedler, F. Schaarschmidt, G. R. Crelier, W. Schwindt, W. Heindel, T. Niederstadt, et al. Magnetic resonance 4D flow characteristics of cerebrospinal fluid at the craniocervical junction and the cervical spinal canal. Eur. Radiol. 21(8):1788–1796, 2011.

    Article  PubMed  Google Scholar 

  9. Clarke, E. C., D. F. Fletcher, M. A. Stoodley, and L. E. Bilston. Computational fluid dynamics modelling of cerebrospinal fluid pressure in Chiari malformation and syringomyelia. J. Biomech. 46(11):1801–1809, 2013.

    Article  PubMed  Google Scholar 

  10. Cushing, H. Studies on the cerebro-spinal fluid: I. Introduction. J. Med. Res. 31(1):1–19, 1914.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Dolar, M. T., V. M. Haughton, B. J. Iskandar, and M. Quigley. Effect of craniocervical decompression on peak CSF velocities in symptomatic patients with Chiari I malformation. Am. J. Neuroradiol. 25(1):142–145, 2004.

    PubMed  Google Scholar 

  12. Glor, F. P., B. Ariff, A. D. Hughes, P. R. Verdonck, S. A. Thom, D. C. Barratt, and X. Y. Xu. Operator dependence of 3-D ultrasound-based computational fluid dynamics for the carotid bifurcation. IEEE Trans. Med. Imaging 24(4):451–456, 2005.

    Article  PubMed  Google Scholar 

  13. Glor, F. P., Q. Long, A. D. Hughes, A. D. Augst, B. Ariff, S. A. Thom, P. R. Verdonck, and X. Y. Xu. Reproducibility study of magnetic resonance image-based computational fluid dynamics prediction of carotid bifurcation flow. Ann. Biomed. Eng. 31(2):142–151, 2003.

    Article  CAS  PubMed  Google Scholar 

  14. Gupta, A., D. Church, D. Barnes, and A. B. Hassan. Cut to the chase: on the need for genotype-specific soft tissue sarcoma trials. Ann. Oncol. 20(3):399–400, 2009.

    Article  CAS  PubMed  Google Scholar 

  15. Gupta, S., M. Soellinger, P. Boesiger, D. Poulikakos, and V. Kurtcuoglu. Three-dimensional computational modeling of subject-specific cerebrospinal fluid flow in the subarachnoid space. J. Biomech. Eng. 131(2):021010, 2009.

    Article  PubMed  Google Scholar 

  16. Gupta, S., M. Soellinger, D. M. Grzybowski, P. Boesiger, J. Biddiscombe, D. Poulikakos, and V. Kurtcuoglu. Cerebrospinal fluid dynamics in the human cranial subarachnoid space: an overlooked mediator of cerebral disease. I. Computational model. J. R. Soc. Interface. 7(49):1195–1204, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Hall, J. E., and A. C. Guyton. Guyton and Hall Textbook of Medical Physiology (12th ed.). Philadelphia: Saunders/Elsevier, p. xix, 2011.

    Google Scholar 

  18. Haughton, V. M., F. R. Korosec, J. E. Medow, M. T. Dolar, and B. J. Iskandar. Peak systolic and diastolic CSF velocity in the foramen magnum in adult patients with Chiari I malformations and in normal control participants. Am. J. Neuroradiol. 24(2):169–176, 2003.

    PubMed  Google Scholar 

  19. Heidari Pahlavian, S., T. Yiallourou, R. S. Tubbs, A. C. Bunck, F. Loth, M. Goodin, et al. The impact of spinal cord nerve roots and denticulate ligaments on cerebrospinal fluid dynamics in the cervical spine. PLoS One 9(4):e91888, 2014. doi:10.1371/journal.pone.0091888.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Helgeland, A., K. A. Mardal, V. Haughton, and B. A. Reif. Numerical simulations of the pulsating flow of cerebrospinal fluid flow in the cervical spinal canal of a Chiari patient. J. Biomech. 47(5):1082–1090, 2014.

    Article  PubMed  Google Scholar 

  21. Henry-Feugeas, M. C., I. Idy-Peretti, O. Baledent, P. Cornu, H. Lejay, J. Bittoun, and A. E. Schouman-Claeys. Cerebrospinal fluid flow waveforms: MR analysis in chronic adult hydrocephalus. Invest. Radiol. 36(3):146–154, 2001.

    Article  CAS  PubMed  Google Scholar 

  22. Hentschel, S., K. A. Mardal, A. E. Lovgren, S. Linge, and V. Haughton. Characterization of cyclic CSF flow in the foramen magnum and upper cervical spinal canal with MR flow imaging and computational fluid dynamics. Am. J. Neuroradiol. 31(6):997–1002, 2010.

    Article  CAS  PubMed  Google Scholar 

  23. Hsu, Y., H. D. Hettiarachchi, D. C. Zhu, and A. A. Linninger. The frequency and magnitude of cerebrospinal fluid pulsations influence intrathecal drug distribution: key factors for interpatient variability (Vol 115, p 386, 2012). Anesth. Analg. 115(4):879, 2012.

    Article  Google Scholar 

  24. Iskandar, B. J., M. Quigley, and V. M. Haughton. Foramen magnum cerebrospinal fluid flow characteristics in children with Chiari I malformation before and after craniocervical decompression. J. Neurosurg. 101(2 Suppl):169–178, 2004.

    PubMed  Google Scholar 

  25. Kurtcuoglu, V., M. Soellinger, P. Summers, K. Boomsma, D. Poulikakos, P. Boesiger, and Y. Ventikos. Computational investigation of subject-specific cerebrospinal fluid flow in the third ventricle and aqueduct of Sylvius. J. Biomech. 40(6):1235–1245, 2007.

    Article  PubMed  Google Scholar 

  26. Kurtcuoglu, V., M. Soellinger, P. Summers, K. Boomsma, D. Poulikakos, P. Boesiger, et al. Reconstruction of cerebrospinal fluid flow in the third ventricle based on MRI data. In: Medical Image Computing and Computer-Assisted Intervention: MICCAI International Conference on Medical Image Computing and Computer-Assisted Intervention, vol. 8(Pt 1), pp. 786–793, 2005.

  27. Linge, S. O., V. Haughton, A. E. Lovgren, K. A. Mardal, A. Helgeland, and H. P. Langtangen. Effect of tonsillar herniation on cyclic CSF flow studied with computational flow analysis. Am. J. Neuroradiol. 32(8):1474–1481, 2011.

    Article  CAS  PubMed  Google Scholar 

  28. Linge, S. O., V. Haughton, A. E. Lovgren, K. A. Mardal, and H. P. Langtangen. CSF flow dynamics at the craniovertebral junction studied with an idealized model of the subarachnoid space and computational flow analysis. Am. J. Neuroradiol. 31(1):185–192, 2010. doi:10.3174/ajnr.A1766.

    Article  CAS  PubMed  Google Scholar 

  29. Linninger, A. A., C. Tsakiris, D. C. Zhu, M. Xenos, P. Roycewicz, Z. Danziger, et al. Pulsatile cerebrospinal fluid dynamics in the human brain. IEEE Trans. Bio Med. Eng. 52(4):557–565, 2005. doi:10.1109/TBME.2005.844021.

    Article  Google Scholar 

  30. Linninger, A. A., M. Xenos, D. C. Zhu, M. R. Somayaji, S. Kondapalli, and R. D. Penn. Cerebrospinal fluid flow in the normal and hydrocephalic human brain. IEEE Trans. Bio Med. Eng. 54(2):291–302, 2007.

    Article  Google Scholar 

  31. Long, Q., B. Ariff, S. Z. Zhao, S. A. Thom, A. D. Hughes, and X. Y. Xu. Reproducibility study of 3D geometrical reconstruction of the human carotid bifurcation from magnetic resonance images. Magn. Reson. Med. 49(4):665–674, 2003.

    Article  CAS  PubMed  Google Scholar 

  32. Loth, F., M. A. Yardimci, and N. Alperin. Hydrodynamic modeling of cerebrospinal fluid motion within the spinal cavity. J. Biomech. Eng. 123(1):71–79, 2001.

    CAS  PubMed  Google Scholar 

  33. Martin, B. A., W. Kalata, F. Loth, T. J. Royston, and J. N. Oshinski. Syringomyelia hydrodynamics: an in vitro study based on in vivo measurements. J. Biomech. Eng. 127(7):1110–1120, 2005.

    Article  PubMed  Google Scholar 

  34. Martin, B. A., W. Kalata, N. Shaffer, P. Fischer, M. Luciano, and F. Loth. Hydrodynamic and longitudinal impedance analysis of cerebrospinal fluid dynamics at the craniovertebral junction in type I Chiari malformation. PLoS One 8(10):e75335, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Martin, B. A., R. Labuda, T. J. Royston, J. N. Oshinski, B. Iskandar, and F. Loth. Spinal subarachnoid space pressure measurements in an in vitro spinal stenosis model: implications on syringomyelia theories. J. Biomech. Eng. 132(11):111007, 2010.

    Article  PubMed  Google Scholar 

  36. Martin, B. A., and F. Loth. The influence of coughing on cerebrospinal fluid pressure in an in vitro syringomyelia model with spinal subarachnoid space stenosis. Cerebrospinal Fluid Res 6:17, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Martin, B. A., P. Reymond, J. Novy, O. Baledent, and N. Stergiopulos. A coupled hydrodynamic model of the cardiovascular and cerebrospinal fluid system. Am. J. Physiol. Heart Circ. Physiol. 302(7):H1492–H1509, 2012.

    Article  CAS  PubMed  Google Scholar 

  38. Matsumae, M., A. Hirayama, H. Atsumi, S. Yatsushiro, and K. Kuroda. Velocity and pressure gradients of cerebrospinal fluid assessed with magnetic resonance imaging. J. Neurosurg. 120(1):218–227, 2014.

    Article  PubMed  Google Scholar 

  39. Moore, J. A., D. A. Steinman, D. W. Holdsworth, and C. R. Ethier. Accuracy of computational hemodynamics in complex arterial geometries reconstructed from magnetic resonance imaging. Ann. Biomed. Eng. 27(1):32–41, 1999.

    Article  CAS  PubMed  Google Scholar 

  40. Pahlavian, S. H., A. C. Bunck, F. Loth, R. S. Tubbs, T. Yiallourou, J. R. Kroeger, et al. Characterization of the discrepancies between four-dimensional phase-contrast magnetic resonance imaging and in-silico simulations of cerebrospinal fluid dynamics. J. Biomech. Eng. 137(5):051002, 2015. doi:10.1115/1.4029699.

    Article  Google Scholar 

  41. Quigley, M. F., B. Iskandar, M. E. Quigley, M. Nicosia, and V. Haughton. Cerebrospinal fluid flow in foramen magnum: temporal and spatial patterns at MR imaging in volunteers and in patients with Chiari I malformation. Radiology 232(1):229–236, 2004.

    Article  PubMed  Google Scholar 

  42. Roldan, A., O. Wieben, V. Haughton, T. Osswald, and N. Chesler. Characterization of CSF hydrodynamics in the presence and absence of tonsillar ectopia by means of computational flow analysis. Am. J. Neuroradiol. 30(5):941–946, 2009.

    Article  CAS  PubMed  Google Scholar 

  43. Sansur, C. A., J. D. Heiss, H. L. DeVroom, E. Eskioglu, R. Ennis, and E. H. Oldfield. Pathophysiology of headache associated with cough in patients with Chiari I malformation. J. Neurosurg. 98(3):453–458, 2003.

    Article  PubMed  Google Scholar 

  44. Shaffer, N., B. Martin, and F. Loth. Cerebrospinal fluid hydrodynamics in type I Chiari malformation. Neurol. Res. 33(3):247–260, 2011.

    Article  PubMed  Google Scholar 

  45. Shaffer, N., B. A. Martin, B. Rocque, C. Madura, O. Wieben, B. Iskandar, et al. Cerebrospinal fluid flow impedance is elevated in type I Chiari malformation. J. Biomech. Eng. 2013. doi:10.1115/1.4026316.

    PubMed  Google Scholar 

  46. Shaffer, N., B. A. Martin, B. Rocque, C. Madura, O. Wieben, B. J. Iskandar, et al. Cerebrospinal fluid flow impedance is elevated in type I Chiari malformation. J. Biomech. Eng. 136(2):021012, 2014. doi:10.1115/1.4026316.

    Article  PubMed  Google Scholar 

  47. Sigmund, E. E., G. A. Suero, C. Hu, K. McGorty, D. K. Sodickson, G. C. Wiggins, and J. A. Helpern. High-resolution human cervical spinal cord imaging at 7 T. NMR Biomed. 25(7):891–899, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Speer, M. C., D. S. Enterline, L. Mehltretter, P. Hammock, J. Joseph, M. Dickerson, R. G. Ellenbogen, T. H. Milhorat, M. A. Hauser, and T. M. George. Review article: chiari type I malformation with or without syringomyelia: prevalence and genetics. J. Genet. Counsel. 12(4):297–311, 2003.

    Article  Google Scholar 

  49. Sweetman, B., and A. A. Linninger. Cerebrospinal fluid flow dynamics in the central nervous system. Ann. Biomed. Eng. 39(1):484–496, 2011.

    Article  PubMed  Google Scholar 

  50. Urbizu, A., M. A. Poca, X. Vidal, A. Rovira, J. Sahuquillo, and A. Macaya. MRI-based morphometric analysis of posterior cranial fossa in the diagnosis of chiari malformation type I. J. Neuroimaging 24(3):250–256, 2014.

    Article  PubMed  Google Scholar 

  51. Williams, B. Further thoughts on valvular action of Arnold-Chiari malformation. Dev. Med. Child Neurol. 6:105–112, 1971.

    Google Scholar 

  52. Williams, B. Simultaneous cerebral and spinal fluid pressure recordings Cerebrospinal dissociation with lesions at the foramen magnum. Acta Neurochir. 59(1–2):123–142, 1981.

    Article  CAS  PubMed  Google Scholar 

  53. Wiswell, T. E., D. J. Tuttle, R. S. Northam, and G. R. Simonds. Major congenital neurologic malformations. A 17-year survey. Am. J. Dis. Child. 144(1):61–67, 1990.

    Article  CAS  PubMed  Google Scholar 

  54. Yiallourou, T. I., J. R. Kroger, N. Stergiopulos, D. Maintz, A. C. Bunck, and B. A. Martin. Comparison of 4D phase-contrast MRI flow measurements to computational fluid dynamics simulations of cerebrospinal fluid motion in the cervical spine. PLoS One 7(12):e52284, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgement

This work was supported by the Swiss National Foundation Grant Nos. 205321_132695/1 and IZK0Z2_152766, NIH R-15 Grant 492 1R15NS071455-01, American Syringomyelia and Chiari Alliance Project and Chiari and Syringomyelia Patient Education Foundation.

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    Authors and Affiliations

    1. Neurophysiological Imaging and Modeling Laboratory, Department of Biological Engineering, The University of Idaho, 875 Perimeter Drive MS 0904, Moscow, ID, 83844-0904, USA

      Bryn A. Martin

    2. Laboratory of Hemodynamics and Cardiovascular Technology, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

      Theresia I. Yiallourou & Nikolaos Stergiopulos

    3. Department of Mechanical Engineering, Conquer Chiari Research Center, The University of Akron, Akron, OH, USA

      Soroush Heidari Pahlavian, Suraj Thyagaraj & Francis Loth

    4. Department of Radiology, University Hospital of Cologne, Cologne, Germany

      Alexander C. Bunck & Jan Robert Kröger

    5. Department of Clinical Radiology, University of Muenster, Münster, Germany

      Alexander C. Bunck & Jan Robert Kröger

    6. Department of Biomedical Engineering, The University of Akron, Akron, OH, USA

      Daniel B. Sheffer

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    Associate Editor Agata Exner oversaw the review of this article.

    Bryn A. Martin and Theresia I. Yiallourou contributed equally to this manuscript.

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    Martin, B.A., Yiallourou, T.I., Pahlavian, S.H. et al. Inter-operator Reliability of Magnetic Resonance Image-Based Computational Fluid Dynamics Prediction of Cerebrospinal Fluid Motion in the Cervical Spine. Ann Biomed Eng 44, 1524–1537 (2016). https://doi.org/10.1007/s10439-015-1449-6

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