Abstract
Chiari malformation type I (CM-I), described by a descent of the cerebellar tonsils, is assumed to be a neurological developmental disorder. The aim of the present study was to investigate morphological variance in cerebellar sub-structures, including gray matter (GM), white matter (WM), and cerebrospinal fluid (CSF), using magnetic resonance (MR) images with three-dimensional (3D) fractal dimension (FD) analysis in patients with CM-I. MRI data of 16 patients and 15 control subjects were obtained, and structural complexity analyses were performed using a box-counting FD algorithm. Results showed that patients with CM-I had significantly reduced FD values for WM and CSF in comparison with controls, and statistically significant differences in cerebellar GM and CSF volumes between patients and controls were found. Moreover, a significant difference was not found between the WM volumes. This may suggest that there are changes in structural complexity in WM even when its volume is unaffected. We conclude that the findings of this preliminary study indicate the possibility of using FD analysis to understand the pathophysiology of CM-I in patients.











Similar content being viewed by others
References
Cai C, Oakes WJ (1997) Hindbrain herniation syndromes: the Chiari malformations (I and II). Semin Pediatr Neurol 4(3):179–191
Bejjani GK (2001) Definition of the adult Chiari malformation: a brief historical overview. Neurosurg Focus 11
Elster AD, Chen MYM (1992) Chiari I malformations: clinical and radiologic reappraisal. Radiology 183:347–353
Osborn AG (1994) Disorders of neural tube closure. In: Diagnostic Neuroradiology (ed) 2. St. Louis Mosby, p 15
Chiari H (1891) Über Veränderungen des Kleinhirns in folge von Hydrocephalie des Grosshirns (in German). Dtsch med Wschr 17:1172–1175
Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Congress of Neurological Surgeons 44(5):1005–1017
Milhorat TH, Nishikawa M, Kula RW, Dlugacz YD (2010) Mechanisms of cerebellar tonsil herniation in patients with Chiari malformations as guide to clinical management. ActaNeurochir (Wien) 152(7):1117–1127
Badie B, Mendoza D, Batzdorf U (1995) Posterior fossa volume and response to suboccipital decompression with Chiari I malformation. Neurosurgery 37:214–218
Nishikawa M, Sakamoto H, Hakuba A, Nakanishi N, Inoue Y (1997) Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 86:40–47
Nyland H, Krogness KG (1978) Size of posterior fossa in Chiari type 1 malformation in adults. Acta Neurochir 40:233–242
Stovner LJ, Bergan U, Nilsen G, Sjaastad O (1993) Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:113–118
Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44(5):1005–1017
Novegno F, Caldarelli M, Massa A, Chieffo D, Massimi L, Pettorini B, Tamburrini G, Di Rocco C (2008) The natural history of the Chiari type I anomaly. J Neurosurg Pediatr 2:179–187
Talal AA, el-Shmam OM (1997) Chiari Malformation Type I: A New MRI Classification. Magn Reson Imaging 15(4):397–403
Carlson MD, Muraszko MK (2003) Chiari I malformation with syrinx. Pediatr Neurol 29(2:167–169
Yassari R, Frim D (2004) Evaluation and management of the Chiari malformation type 1 for the primary care pediatrician. Pediatr Clin N am 51(2):477–490
Lam B, Ryan CF (2000) Arnold-Chiari malformation presenting as sleep apnea syndrome. Sleep med 1:139–144
Kitamura T, Miyazaki S, Kadotani H, Kanemura T, Okawa M, Tanaka T, Komada I, Hatano T, Suzuki H (2014) Type I Chiari malformation presenting central sleep apnea. Auris Nasus Larynx 41(2):222–224
Choi SS, Tran LP, Zalzal GH (1999) Airway abnormalities in patients with Arnold-Chiari malformation. Otolaryngol Head Neck Surg 121(6):720–724
Holinger PC, Holinger LD, Reichert TJ et al (1978) Respiratory obstruction and apnea in infants with bilateral abductor vocal cord paralysis, meningocele, hydrocephalus, and Arnold-Chiari malformation. J Pediatr 92:368–373
Pieh C, Gottlob I (2000) Arnold-Chiari malformation and nystagmus of skew. J Neurol Neurosurg Psychiatry 69:124–126
Staudt MD (2013) Gait disturbances and seizure-like episodes in a patient with a Chiari malformation. UWOMJ. Summer Supplement Issue S1 81:11–12
Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS (2000) Asymptomatic Chiari type I malformations identified on magnetic resonance imaging. J Neurosurg 92:920–926
Speer MC, Enterline DS, Mehltretter L, Hammock P, Joseph J, Dickerson M et al (2003) Chiari type I malformation with or without syringomyelia: prevalence and genetics. J Genet Counsel 12:297–311
Cama A, Tortori-Donati P, Piatelli GL et al (1995) Chiari complex in children—neuroradiological diagnosis, neurosurgical treatment and proposal of a new classification (312 cases). Eur J Pediatr Surg. (suppl 1), 35–8.
Choudhury PR, Sarda P, Baruah P, Singh S (2013) A magnetic resonance imaging study of congenital Chiari malformations. OA Case Reports 2(8):73
Khan AA, Bhatti SN, Khan G, Ahmed E, Aurangzeb A, Ali A, Khan A, Afzal S (2010) Clinical and radiological findings in Arnold Chiari malformation. J Ayub Med Coll Abbottabad 22(2):75–78
Haughton VM, Iskandar BJ (2006) Measuring CSF flow in Chiari I malformations. Neuroradiol J 19:427–432
Navarro R, Olavarria G, Seshadri R, Gonzales-Portillo G, McLone DG, Tomita T (2004) Surgical results of posterior fossa decompression for patients with Chiari I malformation. Childs Nerv Syst 20(5):349–356
Brugieres P, Idy-Peretti I, Iffenecker C et al (2000) CSF flow measurement in syringomyelia. AJNR am J Neuroradiol 21(10):1785–1792
Chang HS, Nakagawa H (2003) Hypothesis on the pathophysiology of syringomyelia based on simulation of cerebrospinal fluid dynamics. J Neurol Neurosurg Psychiatry 74(3):344–347
Clatterbuck RE, Sipos EP (1997) The efficient calculation of neurosurgically relevant volumes from computed tomographic scans using Cavalieri's direct estimator. Neurosurgery 40:339–343
Aydin S, Hanimoglu H, Tanriverdi T, Yentur E, Kaynar MY (2005) Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surg Neurol 64(3):237–241
Clarke EC, Fletcher DF, Stoodley MA, Bilston LE (2011) Computational fluid dynamics modelling of cerebrospinal fluid pressure in Chiari malformation and syringomyelia. J Biomech 46:1801–1809
Ha TH, Yoon U, Lee KJ, Shin YW, Lee JM, Kim IY, Ha KS, Kim SI, Kwon JS (2005) Fractal dimension of cerebral cortical surface in schizophrenia and obsessive–compulsive disorder. Neurosci Lett 384:172–176
Esteban FJ, Sepulcre J, de Mendizábal NV, Goñi J, Navas J, de Miras JR, Bejarano B, Masdeu JC, Villoslada P (2007) Fractal dimension and white matter changes in multiple sclerosis. Neuro Image 36:543–549
Wu YT, Shyu KK, Jao CW, Wang ZY, Soong BW, Wu HM, Wang PS (2010) Fractal dimension analysis for quantifying cerebellar morphological change of multiple system atrophy of the cerebellar type (MSA-C). NeuroImage 49:539–551
Shan ZY, Liu JZ, Glassa JO, Gajjarc A, Lid CS, Reddicka WE (2006) Quantitative morphologic evaluation of white matter in survivors of childhood medulloblastoma. Magn Reson Imaging 24:1015–1022
Free SL, Sisodiya SM, Cook MJ, Fish DR, Shorvon SD (1996) Three dimensional fractal analysis of the white matter surface from magnetic resonance images of the human brain. Cereb Cortex 6:830–836
Liu JZ, Zhang LD, Yue GH (2003) Fractal dimension in human cerebellum measured by magnetic resonance imaging. Biophys J 85:4041–4046
Lee JM, Yoon U, Kim JJ, Kim IY, Lee DS, Kwon JS, Kim SI (2004) Analysis of the hemispheric asymmetry using fractal dimension of a skeletonized cerebral surface. IEEE Trans Biomedical Eng 51:1494–1498
Esteban FJ, Sepulcre J, de Miras JR, Navas J, de Mendizábal NV, Goñi J, Quesada JM, Bejarano B, Villoslada P (2009) Fractal dimension analysis of grey matter in multiple sclerosis. J Neuro Sci 282:67–71
Sandu AL, Rasmussen IA, Lundervold A, Frank Kreuder F, Neckelmann G, Hugdahl K, Specht K (2008) Fractal dimension analysis of MR images reveals grey matter structure irregularities in schizophrenia. Comput med Imaging Graph 32:150–158
Zhao G, Denisova K, Sehatpour P, Long J, Gui W, Qiao J et al (2016) Fractal dimension analysis of subcortical gray matter structures in schizophrenia. PLoS One 11(5):e0155415. doi:10.1371/journal.pone.0155415
Pereira D, Zambrano C, Martin-Landrove M (2000) Evaluation of malignancy in tumors of the central nervous system using fractal dimension. Eng. Med. Biol. Soc. proc. of the 22nd Annu. Intl. Conference of the IEEE 3:1775–1778
Zook JM, Iftekharuddin KM (2005) Statistical analysis of fractal-based brain tumor detection algorithms. Magn Reson Imaging 23:671–678
Takahashi T, Murata T, Omori M, Kosaka H, Takahashi K, Yonekura Y, Wada Y (2004) Quantitative evaluation of age related white matter micro structural changes on MRI by multifractal analysis. J Neurol Sci 225:33–37
Cook MJ (1995) Fractal description of cerebral cortical patterns in frontal-lobe epilepsy. Eur Neurol 35(6):327–335
King RD, George AT, Jeon T, Hynan LS, Youn TS, Kennedy DN, Dickerson B (2009) Characterization of atrophic changes in the cerebral cortex using fractal dimensional analysis. Brain Imaging Behav 3:154–166
Zhang L, Butler AJ, Sun CK, Sahgal V, Wittenberg GF, Yue GH (2008) Fractal dimension assessment of brain white matter structural complexity post stroke in relation to upper-extremity motor function. Brain res 1228:229–240
Zhang L, Yue GH (2016) Fractal dimension studies of the brain shape in aging and neurodegenerative diseases. In Book: the Fractal Geometry of the Brain, pp:213–232. doi:10.1007/978-1-4939-3995-4_14
Akar E, Kara S, Akdemir H, Kırış A (2015) Fractal dimension analysis of cerebellum in Chiari malformation type I. Comput Biol med. doi:10.1016/j.compbiomed.2015.06.024
Ashburner J, Friston KJ, Poline J et al (1995) Spatial registration and normalization of images. Hum Brain Mapp 2:165–189
Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26(3):839–851
NIfTI (2015) Neuroimaging Informatics Technology Initiative http://nifti.nimh.nih.gov/
LONI (2015) Laboratory of Neuro Imaging, ICBM Probabilistic Atlases http://www.loni.usc.edu/ICBM/Downloads/Downloads_ICBMprobabilistic.shtml
Zhang L, Liu JZ, Dean D, Sahgal V, Yue GH (2006) A three-dimensional fractal analysis method for quantifying white matter structure in human brain. J Neurosci Methods 150:242–253
Mandelbrot BB (1983) The fractal geometry of nature. W.H. Freeman, New York
Nezadal M, Zmeskal O, Buchnicek M (2001) The box-counting: critical study. In: Proceedings of the Fourth Conference on Prediction, Synergetic and More 2001:18 (ISBN 80-7318-030-8).
Fernández E, Jelinek HF (2001) Use of fractal theory in neuroscience: methods, advantages, and potential problems. Methods 24(4):309–321
Krishna V, Sammartino F, Yee P, Mikulis D, Walker M, Elias G, Hodaie M (2016) Diffusion tensor imaging assessment of microstructural brainstem integrity in Chiari malformation type I. J Neurosurg 125(5):1112–1119
Ou X, Glasier CM, Snow JH (2011) Diffusion tensor imaging evaluation of white matter in adolescents with myelomeningocele and Chiari II malformation. Pediatr Radiol 41(11):1407–1415. doi:10.1007/s00247-011-2180-6
Lukas C, Schöls L, Bellenberg B, Rüb U, Przuntek H, Schmid G, Koster O, Suchan B (2006) Dissociation of grey and white matter reduction in spinocerebellar ataxia type 3 and 6: a pixel-based morphometry study. Neurosci Lett 408:230–235
Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Markesbery WR (2007) Age and gender effects on human brain anatomy: a pixel-based morphometric study in healthy elderly. Neurobiol Aging 28:1075–1087
Bürk K, Globas C, Wahl T, Bühring U, Diety K, Yühlke C, Luft A, Schuly JB, Voigt K, Dichgans J (2004) MRI-based volumetric differentiation of sporadic cerebellar ataxia. Brain 127:175–181
Napolitano A, Ungania S, Cannata V (2012) Fractal dimension estimation methods for biomedical images, MATLAB-A fundamental tool for scientific computing and engineering applications-volume 3, prof. Vasilios Katsikis (Ed.), InTech, DOI:10.5772/48760.
Annadhason A (2012) Methods of fractal dimension computation. International Journal of Computer Science and Information Technology & Security (IJCSITS) ISSN: 2249–9555 2(1):166–169
Lopes R, Betrouni N (2009) Fractal and multifractal analysis. Med Image Anal 13:634–649
Akar E, Kara S, Akdemir H, Kırış A (2017) Fractal analysis of MR images in patients with chiari malformation: the importance of preprocessing. Biomedical Signal Processing and Control 31:63–70
Acknowledgements
This research was supported by the Fatih University Research and Development Management Office under project number P58011501_B.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Akar, E., Kara, S., Akdemir, H. et al. 3D structural complexity analysis of cerebellum in Chiari malformation type I. Med Biol Eng Comput 55, 2169–2182 (2017). https://doi.org/10.1007/s11517-017-1661-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11517-017-1661-7