- Email: [email protected]
Reduced temporal lobe area in schizophrenia by magnetic resonance imaging: Preliminary evidence
Psychiatry
Research,
261
29126 l-263
Elsevier
Reduced Temporal Lobe Area in Schizophrenia by Magnetic Resonance Imaging: Preliminary Evidence A. Rossi, P. Stratta, L. D’Albenzio, S. Ceccoli, and M. Casacchia
A. Tartaro, G. Schiazza,
V. Di Michele,
Numerous studies over the past 10 years have examined brain morphology of schizophrenics using computed tomography (CT) (Shelton and Weinberger, 1986). The most widely reported finding has been lateral ventricular enlargement (LVE). A recent post-mortem study (Brown et al., 1986) confirming previous reports of ventricular enlargement suggests that such an enlargement is associated with tissue loss in the temporal lobe. In a magnetic resonance imaging (MRI) study, DeLisi et al. ( 1988) reported schizophrenic siblings to have bilateral reduction in the temporal lobe area. Since LVE reported in the majority of cerebral morphological studies is one abnormality, and perhaps the most easily measurable one, the hypothesis is that other cerebral areas such as the temporal or midsagittal structures could be involved in the atrophic/aplasic process appreciated as LVE. We used MRI to examine the morphological characteristics of temporal lobes in a group of schizophrenic patients and normal controls. Fifteen chronic male schizophrenics, diagnosed by DSM-III criteria, were studied with MRI. Their mean age was 26.73 (SD = 4.92) years. The patients had been ill for 4.26 (SD = 2.57) years. They were all being treated with low doses of neuroleptics. MRI scans were also obtained on 11 healthy volunteers who were matched to the patients. Their mean age was 28.36 (SD = 4.98) years. Patients and controls were determined to be right-handed (Oldfield, 1971). MRI examinations were performed using a Philips Gyroscan operating at a 0.5 Tesla magnetic field. A 28-cm crossedellipse head coil was used. The acquisition and reconstruction matrix was 256 X 256. Further methodological details of the scanning procedure have been discussed in another report (Rossi et al., 1988). Briefly, there was one midsagittal cut (5-mm thickness, Spin-Echo 350/30) followed by seven contiguous coronal slices (SE 450/30) which were 8 mm in thickness and perpendicular to the maximum corpus callosum length (MCCL), with slice 1 being the most posterior and slice 7 the most anterior. MCCL was defined as the distance from the most anterior to the most posterior point of the corpus callosum shape in the midsagittal cut. For measurement purposes, all MRI scans were recorded on transparent film that had a magnification of 0.52 times. All linear and area measurements were made by a radiologist who was unaware of the subject’s diagnosis. The radiologist traced the
Reprint requests to: Alessandro Rossi, M.D., Sanita Pubblica, I-7100 L’Aquila, Italy. 0165-178
I /89/$03.50
University of L’Aquila,
@ 1989 Elsevier Scientific
Publishers Ireland
Dipartimento
Ltd.
di Medicine
lnterna e
262 boundaries of the temporal lobes from film onto a digitizing tablet (Graphtec Digitizer, Tokyo) interfaced to an IBM AT. Planimetric measurements were calculated by Autocad software (version 2.64, 1987). To assess test-retest reliability, the same rater digitized the 52 temporal areas at a later date. The two tracings of the temporal lobe size yielded a Pearson r of 0.97. Subsequent calculations used the average of the two measurements. The coronal slice which depicted left and right temporal lobes at their maximum extent was used for measurement purposes. Usually this was slice 4, showing the lateral ventricles, the third ventricle, and the Sylvian fissures. The upper limit of the temporal lobe area was demarcated by a line drawn from the circular sulcus of the insula to the lateral point of the recess dorsolateral to the optic tract. A two-way mixed ANOVA with a between-subjects factor of diagnosis (schizophrenics vs. controls) and a within-subjects factor of hemisphere (left vs. right) was used (Nie et al., 1975) with subsequent t test for unpaired data. The separate variance t test for means was used where appropriate. Pearson product-moment correlations were used for correlation analysis. Area measurements of the temporal lobes are shown in Table 1. Bilateral reduction in the temporal lobe areas was present in the schizophrenic group (p = 0.009) being statistically significant for the left temporal lobe (p = 0.01). There was a significant hemisphere effect (p = 0.03), with the nondominant hemisphere being larger than the dominant hemisphere in both groups. A role for the temporal lobe in schizophrenia has been supported by a recent post-mortem investigation suggesting that lateral ventricular enlargement is most marked in the temporal lobe (Brown et al., 1986); further evidence (from the same sample of brains) localizes the medial temporal lobe as a possible focus of the disease process in schizophrenia (Colter et al., 1987). In the light of the increasing attention being drawn to neuropathological findings, MRI might be used to focus the search for the neuropathological underpinnings of schizophrenia. Our MRI findings are consistent with these post-mortem investigations in suggesting that abnormal growth or atrophy of the temporal lobe, most marked in the left hemisphere, may be one focus of schizophrenic brain pathology. These results give direct support to the concept recently reviewed by Crow (1986) of a disturbance in the left hemisphere, perhaps particularly in temporal structures. From a methodological point of view, MRI is replacing CT as the primary radiologic modality in the evaluation of patients with suspected temporal lobe abnormalities (Latack et al., 1986). MRl has been found superior to CT in displaying normal and abnormal temporal lobe anatomy Table 1. MRI area measurements controls
(square millimeters)
Schizophrenics (n =15)
in schizophrenics
Controls (n =ll)
and
Two-tailed t test
Coronal slice
Mean
SD
Mean
SD
t
P
Right temporal
434.59
48.18
477.27
60.88
1.99
0.058
409.82
29.43
460.89
52.82
2.89
0.011
Left temporal
lobe area lobe area
Two-way ANOVA results: Diagnosis factor F = 8.00; df = 1, 24; p = 0.009. hemisphere factor f = 4.89; df = 1, 24; p = 0.037, interaction NS.
263 because of freedom from bone artifact in the middle cranial fossa, superior soft tissue contrast, and the ability to produce direct coronal images. Gross visual estimation of relative left-right temporal lobe area and thus assessment of unilateral atrophy are ideal in the coronal projection (Clifford et al., 1988) so that MRI is superior for the “in vivo” imaging of the temporal lobe (Naidich et al., 1987). Although we are aware that the brain elements involved in schizophrenia cannot be determined by morphometric observations alone, MRI findings of temporal structures constitute the best view available for an “in vivo” investigation of the schizophrenic brain.
References Brown, R.; Colter, N.; Corsellis, J.A.N.; Crow, T.J.; Frith, C.D.; Jagoe, R.; Johnstone, E.C.; and Marsh, L. Postmortem evidence of structural brain changes in schizophrenia. Archives of General Psychiatry, 43:36, 1986. Clifford, R.; Jack, J.R.; Dale, G.; et al. Temporal lobe volume measurement from MR images: Accuracy and left-right asymmetry in normal persons. Journal of Computer Assisted Tomography, 12:21, 1988. Colter, N.; Battal, S.; Crow, T.J.; Johnstone, E.C.; Brown, R.; and Bruton, C. White matter reduction in the parahippocampal gyrus of patients with schizophrenia. Archives of General Psychiatry, 44: 1023, 1987. Crow, T.J. Left brain, retrotransposons, and schizophrenia. British Medical Journal, 293:3, 1986. DeLisi, L.E.; Alexandropolous, A.; Colter, N.; Crow, T.J.; Dauphinais, D.; Frith, C.; and Gershon, E.S. Reduced temporal lobe area: An MRI study of siblings with schizophrenia. Schizophrenia Research, I : 169, 1988. Latack, J.T.; Abou-Khalili, B.W.; Siegel, G.J.; et al. Patients with partial seizures: Evaluation by MR, CT and PET imaging. Radiology, 159: 159, 1986. Naidich, T.P.; Daniels, D.; Haughton, V.M.; Williams, A.; Pojunas, K.; and Palacios, E. Hippocampal formation and related structures of the limbic lobe: Anatomic-MR correlation. Part I. Surface features and coronal section. Radiology, 162:747, 1987. Nie, N.H.; Hull, C.H.; Jenkins, G.J.; Steinbrenner, K.; and Bent, D.H. SfSS: Statistical Package for the Social Sciences. 2nd ed. New York: McGraw-Hill International Book Co., 1975. Oldfield, R.C. The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9:97, I97 I. Rossi, A.; Stratta, P.; Gallucci, M.; Passariello, R.; and Casacchia, M. Brain morphology in schizophrenia by magnetic resonance imaging (MRI). Acta Psychiatrica Scandinavica. 77:741, 1988. Shelton, R.C., and Weinberger, D.R. X-ray computerized tomography studies in schizophrenia: A review and synthesis. In: Nasrallah, H.A., and Weinberger, D.R., eds. The Neurology of Schizophrenia. Amsterdam: Elsevier, 1986.
Research,
261
29126 l-263
Elsevier
Reduced Temporal Lobe Area in Schizophrenia by Magnetic Resonance Imaging: Preliminary Evidence A. Rossi, P. Stratta, L. D’Albenzio, S. Ceccoli, and M. Casacchia
A. Tartaro, G. Schiazza,
V. Di Michele,
Numerous studies over the past 10 years have examined brain morphology of schizophrenics using computed tomography (CT) (Shelton and Weinberger, 1986). The most widely reported finding has been lateral ventricular enlargement (LVE). A recent post-mortem study (Brown et al., 1986) confirming previous reports of ventricular enlargement suggests that such an enlargement is associated with tissue loss in the temporal lobe. In a magnetic resonance imaging (MRI) study, DeLisi et al. ( 1988) reported schizophrenic siblings to have bilateral reduction in the temporal lobe area. Since LVE reported in the majority of cerebral morphological studies is one abnormality, and perhaps the most easily measurable one, the hypothesis is that other cerebral areas such as the temporal or midsagittal structures could be involved in the atrophic/aplasic process appreciated as LVE. We used MRI to examine the morphological characteristics of temporal lobes in a group of schizophrenic patients and normal controls. Fifteen chronic male schizophrenics, diagnosed by DSM-III criteria, were studied with MRI. Their mean age was 26.73 (SD = 4.92) years. The patients had been ill for 4.26 (SD = 2.57) years. They were all being treated with low doses of neuroleptics. MRI scans were also obtained on 11 healthy volunteers who were matched to the patients. Their mean age was 28.36 (SD = 4.98) years. Patients and controls were determined to be right-handed (Oldfield, 1971). MRI examinations were performed using a Philips Gyroscan operating at a 0.5 Tesla magnetic field. A 28-cm crossedellipse head coil was used. The acquisition and reconstruction matrix was 256 X 256. Further methodological details of the scanning procedure have been discussed in another report (Rossi et al., 1988). Briefly, there was one midsagittal cut (5-mm thickness, Spin-Echo 350/30) followed by seven contiguous coronal slices (SE 450/30) which were 8 mm in thickness and perpendicular to the maximum corpus callosum length (MCCL), with slice 1 being the most posterior and slice 7 the most anterior. MCCL was defined as the distance from the most anterior to the most posterior point of the corpus callosum shape in the midsagittal cut. For measurement purposes, all MRI scans were recorded on transparent film that had a magnification of 0.52 times. All linear and area measurements were made by a radiologist who was unaware of the subject’s diagnosis. The radiologist traced the
Reprint requests to: Alessandro Rossi, M.D., Sanita Pubblica, I-7100 L’Aquila, Italy. 0165-178
I /89/$03.50
University of L’Aquila,
@ 1989 Elsevier Scientific
Publishers Ireland
Dipartimento
Ltd.
di Medicine
lnterna e
262 boundaries of the temporal lobes from film onto a digitizing tablet (Graphtec Digitizer, Tokyo) interfaced to an IBM AT. Planimetric measurements were calculated by Autocad software (version 2.64, 1987). To assess test-retest reliability, the same rater digitized the 52 temporal areas at a later date. The two tracings of the temporal lobe size yielded a Pearson r of 0.97. Subsequent calculations used the average of the two measurements. The coronal slice which depicted left and right temporal lobes at their maximum extent was used for measurement purposes. Usually this was slice 4, showing the lateral ventricles, the third ventricle, and the Sylvian fissures. The upper limit of the temporal lobe area was demarcated by a line drawn from the circular sulcus of the insula to the lateral point of the recess dorsolateral to the optic tract. A two-way mixed ANOVA with a between-subjects factor of diagnosis (schizophrenics vs. controls) and a within-subjects factor of hemisphere (left vs. right) was used (Nie et al., 1975) with subsequent t test for unpaired data. The separate variance t test for means was used where appropriate. Pearson product-moment correlations were used for correlation analysis. Area measurements of the temporal lobes are shown in Table 1. Bilateral reduction in the temporal lobe areas was present in the schizophrenic group (p = 0.009) being statistically significant for the left temporal lobe (p = 0.01). There was a significant hemisphere effect (p = 0.03), with the nondominant hemisphere being larger than the dominant hemisphere in both groups. A role for the temporal lobe in schizophrenia has been supported by a recent post-mortem investigation suggesting that lateral ventricular enlargement is most marked in the temporal lobe (Brown et al., 1986); further evidence (from the same sample of brains) localizes the medial temporal lobe as a possible focus of the disease process in schizophrenia (Colter et al., 1987). In the light of the increasing attention being drawn to neuropathological findings, MRI might be used to focus the search for the neuropathological underpinnings of schizophrenia. Our MRI findings are consistent with these post-mortem investigations in suggesting that abnormal growth or atrophy of the temporal lobe, most marked in the left hemisphere, may be one focus of schizophrenic brain pathology. These results give direct support to the concept recently reviewed by Crow (1986) of a disturbance in the left hemisphere, perhaps particularly in temporal structures. From a methodological point of view, MRI is replacing CT as the primary radiologic modality in the evaluation of patients with suspected temporal lobe abnormalities (Latack et al., 1986). MRl has been found superior to CT in displaying normal and abnormal temporal lobe anatomy Table 1. MRI area measurements controls
(square millimeters)
Schizophrenics (n =15)
in schizophrenics
Controls (n =ll)
and
Two-tailed t test
Coronal slice
Mean
SD
Mean
SD
t
P
Right temporal
434.59
48.18
477.27
60.88
1.99
0.058
409.82
29.43
460.89
52.82
2.89
0.011
Left temporal
lobe area lobe area
Two-way ANOVA results: Diagnosis factor F = 8.00; df = 1, 24; p = 0.009. hemisphere factor f = 4.89; df = 1, 24; p = 0.037, interaction NS.
263 because of freedom from bone artifact in the middle cranial fossa, superior soft tissue contrast, and the ability to produce direct coronal images. Gross visual estimation of relative left-right temporal lobe area and thus assessment of unilateral atrophy are ideal in the coronal projection (Clifford et al., 1988) so that MRI is superior for the “in vivo” imaging of the temporal lobe (Naidich et al., 1987). Although we are aware that the brain elements involved in schizophrenia cannot be determined by morphometric observations alone, MRI findings of temporal structures constitute the best view available for an “in vivo” investigation of the schizophrenic brain.
References Brown, R.; Colter, N.; Corsellis, J.A.N.; Crow, T.J.; Frith, C.D.; Jagoe, R.; Johnstone, E.C.; and Marsh, L. Postmortem evidence of structural brain changes in schizophrenia. Archives of General Psychiatry, 43:36, 1986. Clifford, R.; Jack, J.R.; Dale, G.; et al. Temporal lobe volume measurement from MR images: Accuracy and left-right asymmetry in normal persons. Journal of Computer Assisted Tomography, 12:21, 1988. Colter, N.; Battal, S.; Crow, T.J.; Johnstone, E.C.; Brown, R.; and Bruton, C. White matter reduction in the parahippocampal gyrus of patients with schizophrenia. Archives of General Psychiatry, 44: 1023, 1987. Crow, T.J. Left brain, retrotransposons, and schizophrenia. British Medical Journal, 293:3, 1986. DeLisi, L.E.; Alexandropolous, A.; Colter, N.; Crow, T.J.; Dauphinais, D.; Frith, C.; and Gershon, E.S. Reduced temporal lobe area: An MRI study of siblings with schizophrenia. Schizophrenia Research, I : 169, 1988. Latack, J.T.; Abou-Khalili, B.W.; Siegel, G.J.; et al. Patients with partial seizures: Evaluation by MR, CT and PET imaging. Radiology, 159: 159, 1986. Naidich, T.P.; Daniels, D.; Haughton, V.M.; Williams, A.; Pojunas, K.; and Palacios, E. Hippocampal formation and related structures of the limbic lobe: Anatomic-MR correlation. Part I. Surface features and coronal section. Radiology, 162:747, 1987. Nie, N.H.; Hull, C.H.; Jenkins, G.J.; Steinbrenner, K.; and Bent, D.H. SfSS: Statistical Package for the Social Sciences. 2nd ed. New York: McGraw-Hill International Book Co., 1975. Oldfield, R.C. The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9:97, I97 I. Rossi, A.; Stratta, P.; Gallucci, M.; Passariello, R.; and Casacchia, M. Brain morphology in schizophrenia by magnetic resonance imaging (MRI). Acta Psychiatrica Scandinavica. 77:741, 1988. Shelton, R.C., and Weinberger, D.R. X-ray computerized tomography studies in schizophrenia: A review and synthesis. In: Nasrallah, H.A., and Weinberger, D.R., eds. The Neurology of Schizophrenia. Amsterdam: Elsevier, 1986.