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Published in: Neuroradiology 7/2008

01-07-2008 | Diagnostic Neuroradiology

Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder

Authors: Woo Suk Tae, Sam Soo Kim, Kang Uk Lee, Eui-Cheol Nam, Keun Woo Kim

Published in: Neuroradiology | Issue 7/2008

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Abstract

Introduction

To validate the usefulness of the packages available for automated hippocampal volumetry, we measured hippocampal volumes using one manual and two recently developed automated volumetric methods.

Methods

The study included T1-weighted magnetic resonance imaging (MRI) of 21 patients with chronic major depressive disorder (MDD) and 20 normal controls. Using coronal turbo field echo (TFE) MRI with a slice thickness of 1.3 mm, the hippocampal volumes were measured using three methods: manual volumetry, surface-based parcellation using FreeSurfer, and individual atlas-based volumetry using IBASPM. In addition, the intracranial cavity volume (ICV) was measured manually.

Results

The absolute left hippocampal volume of the patients with MDD measured using all three methods was significantly smaller than the left hippocampal volume of the normal controls (manual P = 0.029, FreeSurfer P = 0.035, IBASPM P = 0.018). After controlling for the ICV, except for the right hippocampal volume measured using FreeSurfer, both measured hippocampal volumes of the patients with MDD were significantly smaller than the measured hippocampal volumes of the normal controls (right manual P = 0.019, IBASPM P = 0.012; left manual P = 0.003, FreeSurfer P = 0.010, IBASPM P = 0.002),. In the intrarater reliability test, the intraclass correlation coefficients (ICCs) were all excellent (manual right 0.947, left 0.934; FreeSurfer right 1.000, left 1.000; IBASPM right 1.000, left 1.000). In the test of agreement between the volumetric methods, the ICCs were right 0.846 and left 0.848 (manual and FreeSurfer), and right 0.654 and left 0.717 (manual and IBASPM).

Conclusion

The automated hippocampal volumetric methods showed good agreement with manual hippocampal volumetry, but the volume measured using FreeSurfer was 35% larger and the agreement was questionable with IBASPM. Although the automated methods could detect hippocampal atrophy in the patients with MDD, the results indicate that manual hippocampal volumetry is still the gold standard, while the automated volumetric methods need to be improved.
Literature
1.
go back to reference Geuze E, Vermetten E, Bremner JD (2005) MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Mol Psychiatry 10:160–184PubMedCrossRef Geuze E, Vermetten E, Bremner JD (2005) MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Mol Psychiatry 10:160–184PubMedCrossRef
2.
go back to reference Geuze E, Vermetten E, Bremner JD (2005) MR-based in vivo hippocampal volumetrics: 1. Review of methodologies currently employed. Mol Psychiatry 10:147–159PubMedCrossRef Geuze E, Vermetten E, Bremner JD (2005) MR-based in vivo hippocampal volumetrics: 1. Review of methodologies currently employed. Mol Psychiatry 10:147–159PubMedCrossRef
3.
go back to reference Alemán-Gómez Y, Melie-García L, Valdés-Hernandez P (2006) IBASPM: toolbox for automatic parcellation of brain structures. Presented at the 12th Annual Meeting of the Organization for Human Brain Mapping, 11–15 June 2006, Florence, Italy. Available on CD-Rom in NeuroImage, vol. 27, no. 1 Alemán-Gómez Y, Melie-García L, Valdés-Hernandez P (2006) IBASPM: toolbox for automatic parcellation of brain structures. Presented at the 12th Annual Meeting of the Organization for Human Brain Mapping, 11–15 June 2006, Florence, Italy. Available on CD-Rom in NeuroImage, vol. 27, no. 1
4.
go back to reference Carmichael OT, Aizenstein HA, Davis SW, Becker JT, Thompson PM, Meltzer CC, Liu Y (2005) Atlas-based hippocampus segmentation in Alzheimer’s disease and mild cognitive impairment. Neuroimage 27:979–990PubMedCrossRef Carmichael OT, Aizenstein HA, Davis SW, Becker JT, Thompson PM, Meltzer CC, Liu Y (2005) Atlas-based hippocampus segmentation in Alzheimer’s disease and mild cognitive impairment. Neuroimage 27:979–990PubMedCrossRef
5.
go back to reference Chupin M, Mukuna-Bantumbakulu AR, Hasboun D, Bardinet E, Baillet S, Kinkingnehun S, Lemieux L, Dubois B, Garnero L (2007) Anatomically constrained region deformation for the automated segmentation of the hippocampus and the amygdala: method and validation on controls and patients with Alzheimer’s disease. Neuroimage 34:996–1019PubMedCrossRef Chupin M, Mukuna-Bantumbakulu AR, Hasboun D, Bardinet E, Baillet S, Kinkingnehun S, Lemieux L, Dubois B, Garnero L (2007) Anatomically constrained region deformation for the automated segmentation of the hippocampus and the amygdala: method and validation on controls and patients with Alzheimer’s disease. Neuroimage 34:996–1019PubMedCrossRef
6.
go back to reference Csernansky JG, Joshi S, Wang L, Haller JW, Gado M, Miller JP, Grenander U, Miller MI (1998) Hippocampal morphometry in schizophrenia by high dimensional brain mapping. Proc Natl Acad Sci U S A 95:11406–11411PubMedCrossRef Csernansky JG, Joshi S, Wang L, Haller JW, Gado M, Miller JP, Grenander U, Miller MI (1998) Hippocampal morphometry in schizophrenia by high dimensional brain mapping. Proc Natl Acad Sci U S A 95:11406–11411PubMedCrossRef
7.
go back to reference Duchesne S, Pruessner JC, Collins DL (2002) Appearance-based segmentation of medial temporal lobe structures. Neuroimage 17:515–531PubMedCrossRef Duchesne S, Pruessner JC, Collins DL (2002) Appearance-based segmentation of medial temporal lobe structures. Neuroimage 17:515–531PubMedCrossRef
8.
go back to reference 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 33:341–355PubMedCrossRef 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 33:341–355PubMedCrossRef
9.
go back to reference Ghanei A, Soltanian-Zadeh H, Windham JP (1998) Segmentation of the hippocampus from brain MRI using deformable contours. Comput Med Imaging Graph 22:203–216PubMedCrossRef Ghanei A, Soltanian-Zadeh H, Windham JP (1998) Segmentation of the hippocampus from brain MRI using deformable contours. Comput Med Imaging Graph 22:203–216PubMedCrossRef
10.
go back to reference Haller JW, Banerjee A, Christensen GE, Gado M, Joshi SC, Miller MI, Sheline YI, Vannier MW, Csernansky JG (1997) Three-dimensional hippocampal MR morphometry with high-dimensional transformation of a neuroanatomical atlas. Radiology 202:504–510PubMed Haller JW, Banerjee A, Christensen GE, Gado M, Joshi SC, Miller MI, Sheline YI, Vannier MW, Csernansky JG (1997) Three-dimensional hippocampal MR morphometry with high-dimensional transformation of a neuroanatomical atlas. Radiology 202:504–510PubMed
11.
go back to reference Hsu YY, Schuff N, Du AT, Mark K, Zhu X, Hardin D, Weiner MW (2002) Comparison of automated and manual MRI volumetry of hippocampus in normal aging and dementia. J Magn Reson Imaging 16:305–310PubMedCrossRef Hsu YY, Schuff N, Du AT, Mark K, Zhu X, Hardin D, Weiner MW (2002) Comparison of automated and manual MRI volumetry of hippocampus in normal aging and dementia. J Magn Reson Imaging 16:305–310PubMedCrossRef
12.
go back to reference Jack CR Jr (1994) MRI-based hippocampal volume measurements in epilepsy. Epilepsia 35 [Suppl 6]:S21–S29PubMedCrossRef Jack CR Jr (1994) MRI-based hippocampal volume measurements in epilepsy. Epilepsia 35 [Suppl 6]:S21–S29PubMedCrossRef
13.
go back to reference Jack CR Jr, Bentley MD, Twomey CK, Zinsmeister AR (1990) MR imaging-based volume measurements of the hippocampal formation and anterior temporal lobe: validation studies. Radiology 176:205–209PubMed Jack CR Jr, Bentley MD, Twomey CK, Zinsmeister AR (1990) MR imaging-based volume measurements of the hippocampal formation and anterior temporal lobe: validation studies. Radiology 176:205–209PubMed
14.
go back to reference Jack CR Jr, Sharbrough FW, Twomey CK, Cascino GD, Hirschorn KA, Marsh WR, Zinsmeister AR, Scheithauer B (1990) Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. Radiology 175:423–429PubMed Jack CR Jr, Sharbrough FW, Twomey CK, Cascino GD, Hirschorn KA, Marsh WR, Zinsmeister AR, Scheithauer B (1990) Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. Radiology 175:423–429PubMed
15.
go back to reference Jack CR Jr, Theodore WH, Cook M, McCarthy G (1995) MRI-based hippocampal volumetrics: data acquisition, normal ranges, and optimal protocol. Magn Reson Imaging 13:1057–1064PubMedCrossRef Jack CR Jr, Theodore WH, Cook M, McCarthy G (1995) MRI-based hippocampal volumetrics: data acquisition, normal ranges, and optimal protocol. Magn Reson Imaging 13:1057–1064PubMedCrossRef
16.
go back to reference Jack CR Jr, Twomey CK, Zinsmeister AR, Sharbrough FW, Petersen RC, Cascino GD (1989) Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 172:549–554PubMed Jack CR Jr, Twomey CK, Zinsmeister AR, Sharbrough FW, Petersen RC, Cascino GD (1989) Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 172:549–554PubMed
17.
go back to reference Luft AR, Skale JM, Welte D, Kolb R, Klose U (1996) Reliability and exactness of MRI-based volumetry: a phantom study. J Magn Reson Imaging 6:700–704PubMedCrossRef Luft AR, Skale JM, Welte D, Kolb R, Klose U (1996) Reliability and exactness of MRI-based volumetry: a phantom study. J Magn Reson Imaging 6:700–704PubMedCrossRef
18.
go back to reference Devanand DP, Pradhaban G, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton GH, Honig LS, Mayeux R, Stern Y, Tabert MH, de Leon MJ (2007) Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology 68:828–836PubMedCrossRef Devanand DP, Pradhaban G, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton GH, Honig LS, Mayeux R, Stern Y, Tabert MH, de Leon MJ (2007) Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology 68:828–836PubMedCrossRef
19.
go back to reference Grundman M, Sencakova D, Jack CR Jr, Petersen RC, Kim HT, Schultz A, Weiner MF, DeCarli C, DeKosky ST, van Dyck C, Thomas RG, Thal LJ (2002) Alzheimer’s Disease Cooperative Study: brain MRI hippocampal volume and prediction of clinical status in a mild cognitive impairment trial. J Mol Neurosci 19:23–27PubMedCrossRef Grundman M, Sencakova D, Jack CR Jr, Petersen RC, Kim HT, Schultz A, Weiner MF, DeCarli C, DeKosky ST, van Dyck C, Thomas RG, Thal LJ (2002) Alzheimer’s Disease Cooperative Study: brain MRI hippocampal volume and prediction of clinical status in a mild cognitive impairment trial. J Mol Neurosci 19:23–27PubMedCrossRef
20.
go back to reference Jack CR Jr, Petersen RC, Xu YC, O’Brien PC, Smith GE, Ivnik RJ, Boeve BF, Waring SC, Tangalos EG, Kokmen E (1999) Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 52:1397–1403PubMed Jack CR Jr, Petersen RC, Xu YC, O’Brien PC, Smith GE, Ivnik RJ, Boeve BF, Waring SC, Tangalos EG, Kokmen E (1999) Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 52:1397–1403PubMed
21.
go back to reference Pantel J, O’Leary DS, Cretsinger K, Bockholt HJ, Keefe H, Magnotta VA, Andreasen NC (2000) A new method for the in vivo volumetric measurement of the human hippocampus with high neuroanatomical accuracy. Hippocampus 10:752–758PubMedCrossRef Pantel J, O’Leary DS, Cretsinger K, Bockholt HJ, Keefe H, Magnotta VA, Andreasen NC (2000) A new method for the in vivo volumetric measurement of the human hippocampus with high neuroanatomical accuracy. Hippocampus 10:752–758PubMedCrossRef
22.
go back to reference Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, Quinn BT, Salat D, Makris N, Fischl B (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26:1261–1270PubMedCrossRef Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, Quinn BT, Salat D, Makris N, Fischl B (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26:1261–1270PubMedCrossRef
23.
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289PubMedCrossRef Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289PubMedCrossRef
24.
go back to reference Han X, Fischl B (2007) Atlas renormalization for improved brain MR image segmentation across scanner platforms. IEEE Trans Med Imaging 26:479–486PubMedCrossRef Han X, Fischl B (2007) Atlas renormalization for improved brain MR image segmentation across scanner platforms. IEEE Trans Med Imaging 26:479–486PubMedCrossRef
25.
go back to reference Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571PubMed Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571PubMed
26.
27.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef
28.
go back to reference Kruggel F (2006) MRI-based volumetry of head compartments: normative values of healthy adults. Neuroimage 30:1–11PubMedCrossRef Kruggel F (2006) MRI-based volumetry of head compartments: normative values of healthy adults. Neuroimage 30:1–11PubMedCrossRef
29.
go back to reference Lemieux L, Hammers A, Mackinnon T, Liu RS (2003) Automatic segmentation of the brain and intracranial cerebrospinal fluid in T1-weighted volume MRI scans of the head, and its application to serial cerebral and intracranial volumetry. Magn Reson Med 49:872–884PubMedCrossRef Lemieux L, Hammers A, Mackinnon T, Liu RS (2003) Automatic segmentation of the brain and intracranial cerebrospinal fluid in T1-weighted volume MRI scans of the head, and its application to serial cerebral and intracranial volumetry. Magn Reson Med 49:872–884PubMedCrossRef
30.
go back to reference MacLullich AM, Ferguson KJ, Deary IJ, Seckl JR, Starr JM, Wardlaw JM (2002) Intracranial capacity and brain volumes are associated with cognition in healthy elderly men. Neurology 59:169–174PubMed MacLullich AM, Ferguson KJ, Deary IJ, Seckl JR, Starr JM, Wardlaw JM (2002) Intracranial capacity and brain volumes are associated with cognition in healthy elderly men. Neurology 59:169–174PubMed
31.
go back to reference Wolf H, Kruggel F, Hensel A, Wahlund LO, Arendt T, Gertz HJ (2003) The relationship between head size and intracranial volume in elderly subjects. Brain Res 973:74–80PubMedCrossRef Wolf H, Kruggel F, Hensel A, Wahlund LO, Arendt T, Gertz HJ (2003) The relationship between head size and intracranial volume in elderly subjects. Brain Res 973:74–80PubMedCrossRef
32.
go back to reference Eritaia J, Wood SJ, Stuart GW, Bridle N, Dudgeon P, Maruff P, Velakoulis D, Pantelis C (2000) An optimized method for estimating intracranial volume from magnetic resonance images. Magn Reson Med 44:973–977PubMedCrossRef Eritaia J, Wood SJ, Stuart GW, Bridle N, Dudgeon P, Maruff P, Velakoulis D, Pantelis C (2000) An optimized method for estimating intracranial volume from magnetic resonance images. Magn Reson Med 44:973–977PubMedCrossRef
33.
go back to reference Chey J, Na DG, Tae WS, Ryoo JW, Hong SB (2006) Medial temporal lobe volume of nondemented elderly individuals with poor cognitive functions. Neurobiol Aging 27:1269–1279PubMedCrossRef Chey J, Na DG, Tae WS, Ryoo JW, Hong SB (2006) Medial temporal lobe volume of nondemented elderly individuals with poor cognitive functions. Neurobiol Aging 27:1269–1279PubMedCrossRef
34.
go back to reference Duvernoy HM (1991) The human brain: surface, three-dimensional sectional anatomy, and MRI. Springer-Verlag, New York, NY Duvernoy HM (1991) The human brain: surface, three-dimensional sectional anatomy, and MRI. Springer-Verlag, New York, NY
35.
go back to reference Hasboun D, Chantome M, Zouaoui A, Sahel M, Deladoeuille M, Sourour N, Duyme M, Baulac M, Marsault C, Dormont D (1996) MR determination of hippocampal volume: comparison of three methods. AJNR Am J Neuroradiol 17:1091–1098PubMed Hasboun D, Chantome M, Zouaoui A, Sahel M, Deladoeuille M, Sourour N, Duyme M, Baulac M, Marsault C, Dormont D (1996) MR determination of hippocampal volume: comparison of three methods. AJNR Am J Neuroradiol 17:1091–1098PubMed
36.
go back to reference Arndt S, Swayze V, Cizadlo T, O’Leary D, Cohen G, Yuh WT, Ehrhardt JC, Andreasen NC (1994) Evaluating and validating two methods for estimating brain structure volumes: tessellation and simple pixel counting. Neuroimage 1:191–198PubMedCrossRef Arndt S, Swayze V, Cizadlo T, O’Leary D, Cohen G, Yuh WT, Ehrhardt JC, Andreasen NC (1994) Evaluating and validating two methods for estimating brain structure volumes: tessellation and simple pixel counting. Neuroimage 1:191–198PubMedCrossRef
37.
go back to reference Cronbach LJ (1951) Coefficient alpha and the internal structure of tests. Psychometrika 16:297–334CrossRef Cronbach LJ (1951) Coefficient alpha and the internal structure of tests. Psychometrika 16:297–334CrossRef
38.
go back to reference Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310PubMed Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310PubMed
39.
go back to reference Pitman EJG (1939) A note on normal correlation. Biometrica 31:9–12 Pitman EJG (1939) A note on normal correlation. Biometrica 31:9–12
40.
go back to reference Frodl T, Schaub A, Banac S, Charypar M, Jager M, Kummler P, Bottlender R, Zetzsche T, Born C, Leinsinger G, Reiser M, Moller HJ, Meisenzahl EM (2006) Reduced hippocampal volume correlates with executive dysfunctioning in major depression. J Psychiatry Neurosci 31:316–323PubMed Frodl T, Schaub A, Banac S, Charypar M, Jager M, Kummler P, Bottlender R, Zetzsche T, Born C, Leinsinger G, Reiser M, Moller HJ, Meisenzahl EM (2006) Reduced hippocampal volume correlates with executive dysfunctioning in major depression. J Psychiatry Neurosci 31:316–323PubMed
41.
go back to reference Hickie I, Naismith S, Ward PB, Turner K, Scott E, Mitchell P, Wilhelm K, Parker G (2005) Reduced hippocampal volumes and memory loss in patients with early- and late-onset depression. Br J Psychiatry 186:197–202PubMedCrossRef Hickie I, Naismith S, Ward PB, Turner K, Scott E, Mitchell P, Wilhelm K, Parker G (2005) Reduced hippocampal volumes and memory loss in patients with early- and late-onset depression. Br J Psychiatry 186:197–202PubMedCrossRef
42.
go back to reference Neumeister A, Wood S, Bonne O, Nugent AC, Luckenbaugh DA, Young T, Bain EE, Charney DS, Drevets WC (2005) Reduced hippocampal volume in unmedicated, remitted patients with major depression versus control subjects. Biol Psychiatry 57:935–937PubMedCrossRef Neumeister A, Wood S, Bonne O, Nugent AC, Luckenbaugh DA, Young T, Bain EE, Charney DS, Drevets WC (2005) Reduced hippocampal volume in unmedicated, remitted patients with major depression versus control subjects. Biol Psychiatry 57:935–937PubMedCrossRef
43.
go back to reference O’Brien JT, Lloyd A, McKeith I, Gholkar A, Ferrier N (2004) A longitudinal study of hippocampal volume, cortisol levels, and cognition in older depressed subjects. Am J Psychiatry 161:2081–2090PubMedCrossRef O’Brien JT, Lloyd A, McKeith I, Gholkar A, Ferrier N (2004) A longitudinal study of hippocampal volume, cortisol levels, and cognition in older depressed subjects. Am J Psychiatry 161:2081–2090PubMedCrossRef
44.
go back to reference Videbech P, Ravnkilde B (2004) Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 161:1957–1966PubMedCrossRef Videbech P, Ravnkilde B (2004) Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 161:1957–1966PubMedCrossRef
45.
go back to reference Li YJ, Ga SN, Huo Y, Li SY, Gao XG (2007) Characteristics of hippocampal volumes in healthy Chinese from MRI. Neurol Res 29:803–806PubMedCrossRef Li YJ, Ga SN, Huo Y, Li SY, Gao XG (2007) Characteristics of hippocampal volumes in healthy Chinese from MRI. Neurol Res 29:803–806PubMedCrossRef
46.
47.
go back to reference Maller JJ, Daskalakis ZJ, Fitzgerald PB (2007) Hippocampal volumetrics in depression: the importance of the posterior tail. Hippocampus 17:1023–1027PubMedCrossRef Maller JJ, Daskalakis ZJ, Fitzgerald PB (2007) Hippocampal volumetrics in depression: the importance of the posterior tail. Hippocampus 17:1023–1027PubMedCrossRef
Metadata
Title
Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder
Authors
Woo Suk Tae
Sam Soo Kim
Kang Uk Lee
Eui-Cheol Nam
Keun Woo Kim
Publication date
01-07-2008
Publisher
Springer-Verlag
Published in
Neuroradiology / Issue 7/2008
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-008-0383-9

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