Skip to main content
Erschienen in: Neuroradiology 9/2016

05.07.2016 | Paediatric Neuroradiology

Comparison of automated brain volumetry methods with stereology in children aged 2 to 3 years

verfasst von: Kristina N. Mayer, Beatrice Latal, Walter Knirsch, Ianina Scheer, Michael von Rhein, Bettina Reich, Jürgen Bauer, Kerstin Gummel, Neil Roberts, Ruth O’Gorman Tuura

Erschienen in: Neuroradiology | Ausgabe 9/2016

Einloggen, um Zugang zu erhalten

Abstract

Introduction

The accurate and precise measurement of brain volumes in young children is important for early identification of children with reduced brain volumes and an increased risk for neurodevelopmental impairment. Brain volumes can be measured from cerebral MRI (cMRI), but most neuroimaging tools used for cerebral segmentation and volumetry were developed for use in adults and have not been validated in infants or young children. Here, we investigate the feasibility and accuracy of three automated software methods (i.e., SPM, FSL, and FreeSurfer) for brain volumetry in young children and compare the measures with corresponding volumes obtained using the Cavalieri method of modern design stereology.

Methods

Cerebral MRI data were collected from 21 children with a complex congenital heart disease (CHD) before Fontan procedure, at a median age of 27 months (range 20.9–42.4 months). Data were segmented with SPM, FSL, and FreeSurfer, and total intracranial volume (ICV) and total brain volume (TBV) were compared with corresponding measures obtained using the Cavalieri method.

Results

Agreement between the estimated brain volumes (ICV and TBV) relative to the gold standard stereological volumes was strongest for FreeSurfer (p < 0.001) and moderate for SPM segment (ICV p = 0.05; TBV p = 0.006). No significant association was evident between ICV and TBV obtained using SPM NewSegment and FSL FAST and the corresponding stereological volumes.

Conclusions

FreeSurfer provides an accurate method for measuring brain volumes in young children, even in the presence of structural brain abnormalities.
Literatur
1.
Zurück zum Zitat Khalil A, Suff N, Thilaganathan B, Hurrell A, Cooper D, Carvalho JS (2014) Brain abnormalities and neurodevelopmental delay in congenital heart disease: systematic review and meta-analysis. Ultrasound Obstet Gynecol 43:14–24CrossRefPubMed Khalil A, Suff N, Thilaganathan B, Hurrell A, Cooper D, Carvalho JS (2014) Brain abnormalities and neurodevelopmental delay in congenital heart disease: systematic review and meta-analysis. Ultrasound Obstet Gynecol 43:14–24CrossRefPubMed
2.
Zurück zum Zitat Owen M, Shevell M, Donofrio M, Majnemer A, McCarter R, Vezina G, Bouyssi-Kobar M, Evangelou I, Freeman D, Weisenfeld N, Limperopoulos C (2014) Brain volume and neurobehavior in newborns with complex congenital heart defects. J Pediatr 164:1121–1127.e1121CrossRefPubMed Owen M, Shevell M, Donofrio M, Majnemer A, McCarter R, Vezina G, Bouyssi-Kobar M, Evangelou I, Freeman D, Weisenfeld N, Limperopoulos C (2014) Brain volume and neurobehavior in newborns with complex congenital heart defects. J Pediatr 164:1121–1127.e1121CrossRefPubMed
3.
Zurück zum Zitat Watanabe K, Matsui M, Matsuzawa J, Tanaka C, Noguchi K, Yoshimura N, Hongo K, Ishiguro M, Wanatabe S, Hirono K, Uese K, Ichida F, Origasa H, Nakazawa J, Oshima Y, Miyawaki T, Matsuzaki T, Yagihara T, Bilker W, Gur RC (2009) Impaired neuroanatomic development in infants with congenital heart disease. J Thorac Cardiovasc Surg 137:146–153CrossRefPubMed Watanabe K, Matsui M, Matsuzawa J, Tanaka C, Noguchi K, Yoshimura N, Hongo K, Ishiguro M, Wanatabe S, Hirono K, Uese K, Ichida F, Origasa H, Nakazawa J, Oshima Y, Miyawaki T, Matsuzaki T, Yagihara T, Bilker W, Gur RC (2009) Impaired neuroanatomic development in infants with congenital heart disease. J Thorac Cardiovasc Surg 137:146–153CrossRefPubMed
4.
Zurück zum Zitat von Rhein M, Buchmann A, Hagmann C, Huber R, Klaver P, Knirsch W, Latal B (2014) Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain 137:268–276CrossRef von Rhein M, Buchmann A, Hagmann C, Huber R, Klaver P, Knirsch W, Latal B (2014) Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain 137:268–276CrossRef
5.
Zurück zum Zitat Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194CrossRefPubMed Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194CrossRefPubMed
6.
Zurück zum Zitat Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355CrossRefPubMed Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355CrossRefPubMed
7.
Zurück zum Zitat Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219CrossRefPubMed Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219CrossRefPubMed
8.
Zurück zum Zitat Ashburner J, Friston KJ (1999) Nonlinear spatial normalization using basis functions. Hum Brain Mapp 7:254–266CrossRefPubMed Ashburner J, Friston KJ (1999) Nonlinear spatial normalization using basis functions. Hum Brain Mapp 7:254–266CrossRefPubMed
9.
Zurück zum Zitat Gousias IS, Rueckert D, Heckemann RA, Dyet LE, Boardman JP, Edwards AD, Hammers A (2008) Automatic segmentation of brain MRIs of 2-year-olds into 83 regions of interest. Neuroimage 40:672–684CrossRefPubMed Gousias IS, Rueckert D, Heckemann RA, Dyet LE, Boardman JP, Edwards AD, Hammers A (2008) Automatic segmentation of brain MRIs of 2-year-olds into 83 regions of interest. Neuroimage 40:672–684CrossRefPubMed
10.
Zurück zum Zitat Murgasova M, Dyet L, Edwards D, Rutherford M, Hajnal J, Rueckert D (2007) Segmentation of brain MRI in young children. Acad Radiol 14:1350–1366CrossRefPubMed Murgasova M, Dyet L, Edwards D, Rutherford M, Hajnal J, Rueckert D (2007) Segmentation of brain MRI in young children. Acad Radiol 14:1350–1366CrossRefPubMed
11.
Zurück zum Zitat Heckemann RA, Hajnal JV, Aljabar P, Rueckert D, Hammers A (2006) Automatic anatomical brain MRI segmentation combining label propagation and decision fusion. Neuroimage 33:115–126CrossRefPubMed Heckemann RA, Hajnal JV, Aljabar P, Rueckert D, Hammers A (2006) Automatic anatomical brain MRI segmentation combining label propagation and decision fusion. Neuroimage 33:115–126CrossRefPubMed
12.
Zurück zum Zitat McQuillen PS, Miller SP (2010) Congenital heart disease and brain development. Ann N Y Acad Sci 1184:68–86CrossRefPubMed McQuillen PS, Miller SP (2010) Congenital heart disease and brain development. Ann N Y Acad Sci 1184:68–86CrossRefPubMed
13.
Zurück zum Zitat Bartholomeusz HH, Courchesne E, Karns CM (2002) Relationship between head circumference and brain volume in healthy normal toddlers, children, and adults. Neuropediatrics 33:239–241CrossRefPubMed Bartholomeusz HH, Courchesne E, Karns CM (2002) Relationship between head circumference and brain volume in healthy normal toddlers, children, and adults. Neuropediatrics 33:239–241CrossRefPubMed
14.
Zurück zum Zitat Ashburner J, Friston K (1997) Multimodal image coregistration and partitioning--a unified framework. Neuroimage 6:209–217CrossRefPubMed Ashburner J, Friston K (1997) Multimodal image coregistration and partitioning--a unified framework. Neuroimage 6:209–217CrossRefPubMed
16.
Zurück zum Zitat Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le Goualher G, Boomsma D, Cannon T, Kawashima R, Mazoyer B (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322CrossRefPubMedPubMedCentral Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le Goualher G, Boomsma D, Cannon T, Kawashima R, Mazoyer B (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat AC E (1993) 3D statistical neuroanatomical models from 305 MRI volumes. In: DL C (ed). Proc. IEEE Nucl. Sci. Symp. Med. Imaging Conf., pp 1813–1817. AC E (1993) 3D statistical neuroanatomical models from 305 MRI volumes. In: DL C (ed). Proc. IEEE Nucl. Sci. Symp. Med. Imaging Conf., pp 1813–1817.
18.
19.
Zurück zum Zitat Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45–57CrossRefPubMed Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45–57CrossRefPubMed
20.
Zurück zum Zitat Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980CrossRefPubMed Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980CrossRefPubMed
21.
Zurück zum Zitat Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207CrossRefPubMed Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207CrossRefPubMed
22.
Zurück zum Zitat Fischl B, van der Kouwe A, Destrieux C, Halgren E, Ségonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22CrossRefPubMed Fischl B, van der Kouwe A, Destrieux C, Halgren E, Ségonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22CrossRefPubMed
23.
Zurück zum Zitat Ségonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26:518–529CrossRefPubMed Ségonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26:518–529CrossRefPubMed
24.
Zurück zum Zitat Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97CrossRefPubMed Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97CrossRefPubMed
25.
Zurück zum Zitat Lowe JR, Maclean PC, Caprihan A, Ohls RK, Qualls C, Vanmeter J, Phillips JP (2012) Comparison of cerebral volume in children aged 18–22 and 36–47 months born preterm and term. J Child Neurol 27:172–177CrossRefPubMed Lowe JR, Maclean PC, Caprihan A, Ohls RK, Qualls C, Vanmeter J, Phillips JP (2012) Comparison of cerebral volume in children aged 18–22 and 36–47 months born preterm and term. J Child Neurol 27:172–177CrossRefPubMed
26.
Zurück zum Zitat Roberts N, Puddephat MJ, McNulty V (2000) The benefit of stereology for quantitative radiology. Br J Radiol 73:679–697CrossRefPubMed Roberts N, Puddephat MJ, McNulty V (2000) The benefit of stereology for quantitative radiology. Br J Radiol 73:679–697CrossRefPubMed
27.
Zurück zum Zitat Puddephat MJ (1999) Computer interface for convenient application for stereological methods for unbiased estimation of volume and surface area: studies using MRI with particular reference to the human brain. University of Liverpool, Liverpool Puddephat MJ (1999) Computer interface for convenient application for stereological methods for unbiased estimation of volume and surface area: studies using MRI with particular reference to the human brain. University of Liverpool, Liverpool
28.
Zurück zum Zitat Keller SS, Highley JR, Garcia-Finana M, Sluming V, Rezaie R, Roberts N (2007) Sulcal variability, stereological measurement and asymmetry of Broca’s area on MR images. J Anat 211:534–555PubMedPubMedCentral Keller SS, Highley JR, Garcia-Finana M, Sluming V, Rezaie R, Roberts N (2007) Sulcal variability, stereological measurement and asymmetry of Broca’s area on MR images. J Anat 211:534–555PubMedPubMedCentral
29.
Zurück zum Zitat Keller SS, Gerdes JS, Mohammadi S, Kellinghaus C, Kugel H, Deppe K, Ringelstein EB, Evers S, Schwindt W, Deppe M (2012) Volume estimation of the thalamus using freesurfer and stereology: consistency between methods. Neuroinformatics 10:341–350CrossRefPubMedPubMedCentral Keller SS, Gerdes JS, Mohammadi S, Kellinghaus C, Kugel H, Deppe K, Ringelstein EB, Evers S, Schwindt W, Deppe M (2012) Volume estimation of the thalamus using freesurfer and stereology: consistency between methods. Neuroinformatics 10:341–350CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Cruz-Orive LM, Gelšvartas J, Roberts N (2014) Sampling theory and automated simulations for vertical sections, applied to human brain. J Microsc 253:119–150CrossRefPubMed Cruz-Orive LM, Gelšvartas J, Roberts N (2014) Sampling theory and automated simulations for vertical sections, applied to human brain. J Microsc 253:119–150CrossRefPubMed
31.
Zurück zum Zitat Mayhew TM, Olsen DR (1991) Magnetic resonance imaging (MRI) and model-free estimates of brain volume determined using the Cavalieri principle. J Anat 178:133–144PubMedPubMedCentral Mayhew TM, Olsen DR (1991) Magnetic resonance imaging (MRI) and model-free estimates of brain volume determined using the Cavalieri principle. J Anat 178:133–144PubMedPubMedCentral
32.
Zurück zum Zitat Keller SS, Roberts N (2009) Measurement of brain volume using MRI: software, techniques, choices and prerequisites. J Anthropol Sci 87:127–151PubMed Keller SS, Roberts N (2009) Measurement of brain volume using MRI: software, techniques, choices and prerequisites. J Anthropol Sci 87:127–151PubMed
33.
Zurück zum Zitat Salmenperä T, Könönen M, Roberts N, Vanninen R, Pitkänen A, Kälviäinen R (2005) Hippocampal damage in newly diagnosed focal epilepsy: a prospective MRI study. Neurology 64:62–68CrossRefPubMed Salmenperä T, Könönen M, Roberts N, Vanninen R, Pitkänen A, Kälviäinen R (2005) Hippocampal damage in newly diagnosed focal epilepsy: a prospective MRI study. Neurology 64:62–68CrossRefPubMed
34.
Zurück zum Zitat Mulder ER, de Jong RA, Knol DL, van Schijndel RA, Cover KS, Visser PJ, Barkhof F, Vrenken H, Initiative ADN (2014) Hippocampal volume change measurement: quantitative assessment of the reproducibility of expert manual outlining and the automated methods FreeSurfer and FIRST. Neuroimage 92:169–181CrossRefPubMed Mulder ER, de Jong RA, Knol DL, van Schijndel RA, Cover KS, Visser PJ, Barkhof F, Vrenken H, Initiative ADN (2014) Hippocampal volume change measurement: quantitative assessment of the reproducibility of expert manual outlining and the automated methods FreeSurfer and FIRST. Neuroimage 92:169–181CrossRefPubMed
35.
Zurück zum Zitat Eggert LD, Sommer J, Jansen A, Kircher T, Konrad C (2012) Accuracy and reliability of automated gray matter segmentation pathways on real and simulated structural magnetic resonance images of the human brain. PLoS One 7:e45081CrossRefPubMedPubMedCentral Eggert LD, Sommer J, Jansen A, Kircher T, Konrad C (2012) Accuracy and reliability of automated gray matter segmentation pathways on real and simulated structural magnetic resonance images of the human brain. PLoS One 7:e45081CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Morey RA, Petty CM, Xu Y, Hayes JP, Wagner HR, Lewis DV, LaBar KS, Styner M, McCarthy G (2009) A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 45:855–866CrossRefPubMed Morey RA, Petty CM, Xu Y, Hayes JP, Wagner HR, Lewis DV, LaBar KS, Styner M, McCarthy G (2009) A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 45:855–866CrossRefPubMed
37.
Zurück zum Zitat Klauschen F, Goldman A, Barra V, Meyer-Lindenberg A, Lundervold A (2009) Evaluation of automated brain MR image segmentation and volumetry methods. Hum Brain Mapp 30:1310–1327CrossRefPubMed Klauschen F, Goldman A, Barra V, Meyer-Lindenberg A, Lundervold A (2009) Evaluation of automated brain MR image segmentation and volumetry methods. Hum Brain Mapp 30:1310–1327CrossRefPubMed
38.
Zurück zum Zitat Dewey J, Hana G, Russell T, Price J, McCaffrey D, Harezlak J, Sem E, Anyanwu JC, Guttmann CR, Navia B, Cohen R, Tate DF, Consortium HN (2010) Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study. Neuroimage 51:1334–1344CrossRefPubMedPubMedCentral Dewey J, Hana G, Russell T, Price J, McCaffrey D, Harezlak J, Sem E, Anyanwu JC, Guttmann CR, Navia B, Cohen R, Tate DF, Consortium HN (2010) Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study. Neuroimage 51:1334–1344CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Furlong C, García-Fiñana M, Puddephat M, Anderson A, Fabricius K, Eriksen N, Pakkenberg B, Roberts N (2013) Application of stereological methods to estimate post-mortem brain surface area using 3T MRI. Magn Reson Imaging 31:456–465CrossRefPubMed Furlong C, García-Fiñana M, Puddephat M, Anderson A, Fabricius K, Eriksen N, Pakkenberg B, Roberts N (2013) Application of stereological methods to estimate post-mortem brain surface area using 3T MRI. Magn Reson Imaging 31:456–465CrossRefPubMed
40.
Zurück zum Zitat Medoff-Cooper B, Irving SY, Hanlon AL, Golfenshtein N, Radcliffe J, Stallings VA, Marino BS, Ravishankar C (2016) The association among feeding mode, growth, and developmental outcomes in infants with complex congenital heart disease at 6 and 12 months of Age. J Pediatr 169:154–159.e151CrossRefPubMed Medoff-Cooper B, Irving SY, Hanlon AL, Golfenshtein N, Radcliffe J, Stallings VA, Marino BS, Ravishankar C (2016) The association among feeding mode, growth, and developmental outcomes in infants with complex congenital heart disease at 6 and 12 months of Age. J Pediatr 169:154–159.e151CrossRefPubMed
41.
Zurück zum Zitat Daymont C, Neal A, Prosnitz A, Cohen MS (2013) Growth in children with congenital heart disease. Pediatrics 131:e236–e242CrossRefPubMed Daymont C, Neal A, Prosnitz A, Cohen MS (2013) Growth in children with congenital heart disease. Pediatrics 131:e236–e242CrossRefPubMed
Metadaten
Titel
Comparison of automated brain volumetry methods with stereology in children aged 2 to 3 years
verfasst von
Kristina N. Mayer
Beatrice Latal
Walter Knirsch
Ianina Scheer
Michael von Rhein
Bettina Reich
Jürgen Bauer
Kerstin Gummel
Neil Roberts
Ruth O’Gorman Tuura
Publikationsdatum
05.07.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Neuroradiology / Ausgabe 9/2016
Print ISSN: 0028-3940
Elektronische ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-016-1714-x

Weitere Artikel der Ausgabe 9/2016

Neuroradiology 9/2016 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.