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The Anatomy of First-Episode and Chronic Schizophrenia: an Anatomical Likelihood Estimation Meta-Analysis

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The Anatomy of First-Episode and Chronic Schizophrenia: an Anatomical Likelihood Estimation Meta-Analysis Article The Anatomy of First-Episode and Chronic Schizophrenia: An Anatomical Likelihood Estimation Meta-Analysis Ian Ellison-Wright, M.R.C.P. Objective: The authors sought to map schizophrenia and chronic schizophrenia, gray matter changes in first-episode including gray matter decreases in the David C. Glahn, Ph.D. schizophrenia and to compare these with thalamus, the left uncus/amygdala re- the changes in chronic schizophrenia. gion, the insula bilaterally, and the ante- They postulated that the data would rior cingulate. In the comparison of first- Angela R. Laird, Ph.D. show a progression of changes from hip- episode schizophrenia and chronic pocampal deficits in first-episode schizo- schizophrenia, decreases in gray matter Sarah M. Thelen, B.S. phrenia to include volume reductions in volume were detected in first-episode the amygdala and cortical gray matter in schizophrenia but not in chronic schizo- Ed Bullmore, Ph.D. chronic schizophrenia. phrenia in the caudate head bilaterally; decreases were more widespread in corti- Method: A systematic search was con- cal regions in chronic schizophrenia. ducted for voxel-based structural MRI studies of patients with first-episode Conclusions: Anatomical changes in schizophrenia and chronic schizophrenia first-episode schizophrenia broadly coin- in relation to comparison groups. Meta- cide with a basal ganglia-thalamocortical analyses of the coordinates of gray matter circuit. These changes include bilateral re- differences were carried out using ana- ductions in caudate head gray matter, tomical likelihood estimation. Maps of which are absent in chronic schizophre- gray matter changes were constructed, nia. Comparing first-episode schizophre- and subtraction meta-analysis was used nia and chronic schizophrenia, the au- to compare them. thors did not find evidence for the temporolimbic progression of pathology Results: A total of 27 articles were identi- from hippocampus to amygdala, but fied for inclusion in the meta-analyses. A there was evidence for progression of cor- marked correspondence was observed in tical changes. regions affected by both first-episode (Am J Psychiatry 2008; 165:1015–1023) The anatomical brain changes in first-episode schizo- Other volumes that were smaller were the hippocampus phrenia are of interest for at least three reasons: 1) they (93% on the left and 94% on the right), the parahippo- may indicate a progression of brain changes after disease campi (92% on the left and 89% on the right), the onset, 2) they may represent the core regions of patholog- amygdala (91% on both sides), the frontal lobes (97% on ical change in schizophrenia, and 3) they may provide a both sides), and the temporal lobes (98% on the left and key to earlier diagnosis. 97% on the right) (5). Changes in brain structure in first-episode schizophre- If there are more widespread brain changes in chronic nia have been identified by meta-analyses of MRI studies schizophrenia than in first-episode schizophrenia, then (1–3). Compared with matched comparison groups, pa- this could imply a progression of brain anatomical tients were found to have reduced whole brain volume changes after symptom onset. Since hippocampal deficits, (97%) and increased lateral ventricular volume (134% on but not amygdala deficits, appear to be present in first-ep- the right and 125% on the left). In patients, hippocampal isode schizophrenia, this has led to the hypothesis that volumes were 92% on both sides (1). However, amygdala there is a progression of temporolimbic involvement after volumes and temporal lobe volumes were not significantly disease onset (3). Furthermore, if there are more localized different (3). changes in first-episode schizophrenia, then these may These changes may be less widespread than those in represent the core regions of pathology (or neurodevelop- chronic schizophrenia. Meta-analyses that included mental abnormality). They may represent the critical mainly patients with chronic schizophrenia (4–6) found nodes in neurochemical circuits whose continuing dys- that patients also had smaller mean cerebral volumes function leads to further anatomical changes within the (98%) and greater total ventricular volumes (126%). circuits over time. This article is featured in this month’s AJP Audio and is discussed in an editorial by Drs. Csernansky and Cronenwett (p. 937) and in an editorial by Dr. Tamminga (p. 949). Am J Psychiatry 165:8, August 2008 ajp.psychiatryonline.org 1015 ANATOMY OF FIRST-EPISODE AND CHRONIC SCHIZOPHRENIA Finally, the identification of specific anatomical brain A previous meta-analysis of gray matter changes in changes in first-episode schizophrenia could provide a schizophrenia (including mainly studies of chronic key to earlier diagnosis. Studies of brain MR images in in- schizophrenia) found that deficits in patients were more dividuals at high risk of developing a psychotic disorder frequently observed in various cortical and subcortical re- have found gray matter changes (7, 8), and it is important gions, including the superior temporal gyrus bilaterally, to define which of these changes are indicative of first-ep- the medial frontal gyrus bilaterally, the anterior cingulate, isode schizophrenia. There is some evidence that earlier the insular cortex bilaterally, the parahippocampal gyrus diagnosis and treatment of schizophrenia lead to im- bilaterally, the thalamus, and the caudate bilaterally (17). proved outcomes (9, 10). The objectives of this meta-analysis were to use ALE to In this study, we conducted meta-analyses of voxel- investigate gray matter structural brain changes in first- based morphometry imaging studies by applying the episode schizophrenia and to compare the distribution of technique of activation likelihood estimation (11). Activa- these changes with those in chronic schizophrenia. We hy- tion likelihood estimation was originally developed to pothesized that ALE analysis of first-episode schizophre- identify the brain regions that were consistently activated nia studies would 1) identify the hippocampi but not the by a cognitive task (12, 13), using coordinates reported by amygdala as regions affected by first-episode schizophre- different functional imaging studies. It assumes that al- nia and 2) demonstrate more widespread cortical changes though each study reported the specific coordinates of ac- in chronic schizophrenia compared with first-episode tivations, technical issues (such as interindividual vari- schizophrenia. ability in brain anatomy) and differences in investigators’ labels for anatomical regions lead to some uncertainty as Method to the actual locations of these peaks. Therefore, activa- tion foci do not represent single points but rather “local- Study Ascertainment ization probability distributions” centered on the particu- Studies were considered for inclusion if they were published lar coordinates. In activation likelihood estimation, the before June 2007 in article format (rather than as letters or ab- stracts), if they compared a group of subjects with schizophrenia foci reported by each study are modeled as a probability (or schizophrenia and related diagnoses) and a comparison distribution. Then a map of the whole brain is con- group (either related or unrelated to the subjects), if they utilized structed, assigning to each voxel a value equal to the prob- voxel-based morphometric analysis of MRI data sets to investi- ability that an activation lies within the voxel. This value is gate differences in whole-brain structure (gray matter density), called the “activation likelihood estimation.” A statistical and if they reported the three-dimensional coordinates of brain changes in stereotactic space. test of these values is then performed by comparing them If measurements were reported for both an unrelated and a re- with values in a null distribution obtained by permutation lated comparison group, then the former measurements were testing, correcting for multiple comparisons by control- used. If the comparison groups were unaffected dizygotic or ling the false discovery rate. For example, a false discovery monozygotic twins, then the former measurements were used rate correction guarantees that in a set of voxels deemed (on the assumption that they showed genetic as well as environ- mental differences). Studies reporting results on a patient group significant for a test of α=0.05, the expected proportion of in which patients had a diagnosis of schizophrenia but some pa- false positives is controlled (11). tients had related diagnoses (e.g., schizoaffective disorder, first- One of the difficulties when comparing imaging studies episode psychosis) were also included. Studies that reported sep- is that there is considerable variability when labeling neu- arate results for male and female subjects were entered as com- bined data. Studies in which the patients’ duration of illness was roanatomical regions, and differences in nomenclature less than 1.5 years (e.g., with early-onset schizophrenia) were could obscure findings. An advantage of the activation classified in the first-episode schizophrenia group. likelihood estimation technique is that because it uses the Study data were excluded if insufficient data were reported to coordinates of reported foci (rather than anatomical la- extract the number of subjects in each group, if there were bels) for meta-analysis, it avoids the problem of any misla- fewer than six subjects in either the schizophrenia group or the comparison group, or if the data contributed to another
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