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

IntroductionTo 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.MethodsThe 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.ResultsThe 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).ConclusionThe 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.

[1]  E. Cabanis,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy and Mri , 1991 .

[2]  C. Jack,et al.  Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. , 1989, Radiology.

[3]  E. Pitman.  A NOTE ON NORMAL CORRELATION , 1939 .

[4]  Stephan Arndt,et al.  Evaluating and Validating Two Methods for Estimating Brain Structure Volumes: Tessellation and Simple Pixel Counting , 1994, NeuroImage.

[5]  M W Vannier,et al.  Three-dimensional hippocampal MR morphometry with high-dimensional transformation of a neuroanatomic atlas. , 1997, Radiology.

[6]  P. Fitzgerald,et al.  Hippocampal volumetrics in depression: The importance of the posterior tail , 2007, Hippocampus.

[7]  A. Dale,et al.  Effects of age on volumes of cortex, white matter and subcortical structures , 2005, Neurobiology of Aging.

[8]  A. Beckett,et al.  AKUFO AND IBARAPA. , 1965, Lancet.

[9]  C R Jack,et al.  Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. , 1990, Radiology.

[10]  Xu-guang Gao,et al.  Characteristics of hippocampal volumes in healthy Chinese from MRI , 2007, Neurological research.

[11]  J. Bremner,et al.  MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders , 2005, Molecular Psychiatry.

[12]  Frithjof Kruggel,et al.  The relationship between head size and intracranial volume in elderly subjects , 2003, Brain Research.

[13]  Dhananjay Ghongade,et al.  Neuroradiology , 2007, Indian Journal of Radiology and Imaging.

[14]  N C Andreasen,et al.  A new method for the in vivo volumetric measurement of the human hippocampus with high neuroanatomical accuracy , 2000, Hippocampus.

[15]  R. Mayeux,et al.  Hippocampal and entorhinal atrophy in mild cognitive impairment , 2007, Neurology.

[16]  Anil Gholkar,et al.  A longitudinal study of hippocampal volume, cortisol levels, and cognition in older depressed subjects. , 2004, The American journal of psychiatry.

[17]  M. Baulac,et al.  MR determination of hippocampal volume: comparison of three methods. , 1996, AJNR. American journal of neuroradiology.

[18]  Dong Gyu Na,et al.  Medial temporal lobe volume of nondemented elderly individuals with poor cognitive functions , 2006, Neurobiology of Aging.

[19]  Alexander Hammers,et al.  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 , 2003, Magnetic resonance in medicine.

[20]  Philip B. Ward,et al.  Reduced hippocampal volumes and memory loss in patients with early- and late-onset depression , 2005, British Journal of Psychiatry.

[21]  L. Cronbach.  Coefficient alpha and the internal structure of tests , 1951 .

[22]  D. Altman,et al.  STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT , 1986, The Lancet.

[23]  U. Grenander,et al.  Hippocampal morphometry in schizophrenia by high dimensional brain mapping. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Frithjof Kruggel,et al.  MRI-based volumetry of head compartments: Normative values of healthy adults , 2006, NeuroImage.

[25]  Paul M. Thompson,et al.  Atlas-based hippocampus segmentation in Alzheimer's disease and mild cognitive impairment , 2005, NeuroImage.

[26]  Dennis S. Charney,et al.  Reduced hippocampal volume in unmedicated, remitted patients with major depression versus control subjects , 2005, Biological Psychiatry.

[27]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[28]  Hans-Jürgen Möller,et al.  Reduced hippocampal volume correlates with executive dysfunctioning in major depression. , 2006, Journal of psychiatry & neuroscience : JPN.

[29]  N. Schuff,et al.  Comparison of automated and manual MRI volumetry of hippocampus in normal aging and dementia , 2002, Journal of magnetic resonance imaging : JMRI.

[30]  Dominique Hasboun,et al.  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 , 2007, NeuroImage.

[31]  C. Jack,et al.  Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment , 1999, Neurology.

[32]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[33]  C. Jack,et al.  Brain MRI hippocampal volume and prediction of clinical status in a mild cognitive impairment trial , 2002, Journal of Molecular Neuroscience.

[34]  C. Jack,et al.  MRI‐Based Hippocampal Volume Measurements in Epilepsy , 1994, Epilepsia.

[35]  U Klose,et al.  Reliability and exactness of MRI‐based volumetry: A phantom study , 1996, Journal of magnetic resonance imaging : JMRI.

[36]  C. Jack,et al.  MR imaging-based volume measurements of the hippocampal formation and anterior temporal lobe: validation studies. , 1990, Radiology.

[37]  J M Bland,et al.  Statistical methods for assessing agreement between two methods of clinical measurement , 1986 .

[38]  Karen J. Ferguson,et al.  Intracranial capacity and brain volumes are associated with cognition in healthy elderly men , 2002, Neurology.

[39]  B. Ravnkilde,et al.  Hippocampal volume and depression: a meta-analysis of MRI studies. , 2004, The American journal of psychiatry.

[40]  Xiao Han,et al.  Atlas Renormalization for Improved Brain MR Image Segmentation Across Scanner Platforms , 2007, IEEE Transactions on Medical Imaging.

[41]  M. Hamilton.  A RATING SCALE FOR DEPRESSION , 1960, Journal of neurology, neurosurgery, and psychiatry.

[42]  P. Maruff,et al.  An optimized method for estimating intracranial volume from magnetic resonance images , 2000, Magnetic resonance in medicine.

[43]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[44]  J. Bremner,et al.  MR-based in vivo hippocampal volumetrics: 1. Review of methodologies currently employed , 2005, Molecular Psychiatry.

[45]  S. Duchesne,et al.  Appearance-Based Segmentation of Medial Temporal Lobe Structures , 2002, NeuroImage.

[46]  C R Jack,et al.  MRI-based hippocampal volumetrics: data acquisition, normal ranges, and optimal protocol. , 1995, Magnetic resonance imaging.

[47]  H Soltanian-Zadeh,et al.  Segmentation of the hippocampus from brain MRI using deformable contours. , 1998, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.