Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-25T00:54:31.271Z Has data issue: false hasContentIssue false
  • English
  • Français

No progression of the alterations in the cortical thickness of individuals with schizophrenia-spectrum disorder: a three-year longitudinal magnetic resonance imaging study of first-episode patients

Published online by Cambridge University Press:  25 May 2015

R. Roiz-Santiáñez ,
V. Ortiz-García de la Foz ,
R. Ayesa-Arriola ,
D. Tordesillas-Gutiérrez ,
R. Jorge ,
N. Varela-Gómez ,
P. Suárez-Pinilla ,
A. Córdova-Palomera ,
J. M. Navasa-Melado  and
B. Crespo-Facorro
R. Roiz-Santiáñez*
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain
V. Ortiz-García de la Foz
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain
R. Ayesa-Arriola
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain
D. Tordesillas-Gutiérrez
Affiliation:
Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain Neuroimaging Unit/Technological Facilities–IDIVAL, Santander, Spain
R. Jorge
Affiliation:
Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, USA
N. Varela-Gómez
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain
P. Suárez-Pinilla
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain
A. Córdova-Palomera
Affiliation:
Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain Departament de Biologia Animal, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain
J. M. Navasa-Melado
Affiliation:
Department of Neuroradiology, University Hospital Marqués de Valdecilla–IDIVAL, Santander, Spain
B. Crespo-Facorro
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Madrid, Spain
*
*Address for correspondence: R. Roiz-Santiáñez, Ph.D., Unidad Investigación Psiquiatría, Hospital Universitario Marqués de Valdecilla, Avda. Valdecilla s/n, 39008, Santander, Spain. (Email: rroiz@humv.es)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Cortical thickness measurement offers an index of brain development processes. In healthy individuals, cortical thickness is reduced with increasing age and is related to cognitive decline. Cortical thinning has been reported in schizophrenia. Whether cortical thickness changes differently over time in patients and its impact on outcome remain unanswered.

Method

Data were examined from 109 patients and 76 healthy controls drawn from the Santander Longitudinal Study of first-episode schizophrenia for whom adequate structural magnetic resonance imaging (MRI) data were available (n = 555 scans). Clinical and cognitive assessments and MRIs were acquired at three regular time points during a 3-year follow-up period. We investigated likely progressive cortical thickness changes in schizophrenia during the first 3 years after initiating antipsychotic treatment. The effects of cortical thickness changes on cognitive and clinical variables were also examined along with the impact of potential confounding factors.

Results

There were significant diagnoses × scan time interaction main effects for total cortical thickness (F1,309.1 = 4.60, p = 0.033) and frontal cortical thickness (F1,310.6 = 5.30, p = 0.022), reflecting a lesser thinning over time in patients. Clinical and cognitive outcome was not associated with progressive cortical changes during the early years of the illness.

Conclusions

Cortical thickness abnormalities do not unswervingly progress, at least throughout the first years of the illness. Previous studies have suggested that modifiable factors may partly account for cortical thickness abnormalities. Therefore, the importance of implementing practical actions that may modify those factors and improve them over the course of the illness should be highlighted.

Keywords

Clinical assessmentcortical thicknessfirst-episode psychosislongitudinal studiesschizophreniastructural magnetic resonance imaging
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 13 , October 2015 , pp. 2861 - 2871
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agartz, I, Okuguwa, G, Nordstrom, M, Greitz, D, Magnotta, V, Sedvall, G (2001). Reliability and reproducibility of brain tissue volumetry from segmented MR scans. European Archives of Psychiatry and Clinical Neuroscience 251, 255–261.Google Scholar
Alexander, GE, Chen, K, Aschenbrenner, M, Merkley, TL, Santerre-Lemmon, LE, Shamy, JL, Skaggs, WE, Buonocore, MH, Rapp, PR, Barnes, CA (2008). Age-related regional network of magnetic resonance imaging gray matter in the rhesus macaque. Journal of Neuroscience 28, 2710–2718.Google Scholar
Andreasen, NC (1983). The Scale for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City.Google Scholar
Andreasen, NC (1984). The Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa: Iowa City.Google Scholar
Andreasen, NC, Flaum, M, Arndt, S (1992). The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. Archives of General Psychiatry 49, 615–623.Google Scholar
Andreasen, NC, Liu, D, Ziebell, S, Vora, A, Ho, BC (2013). Relapse duration, treatment intensity, and brain tissue loss in schizophrenia: a prospective longitudinal MRI study. American Journal of Psychiatry 170, 609–615.Google Scholar
Ayesa-Arriola, R, Perez-Iglesias, R, Rodriguez-Sanchez, JM, Pardo-Garcia, G, Tabares-Seisdedos, R, Ayuso-Mateos, JL, Vazquez-Barquero, JL, Crespo-Facorro, B (2013). Predictors of neurocognitive impairment at 3 years after a first episode non-affective psychosis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 43C, 23–28.Google Scholar
Blix, E, Perski, A, Berglund, H, Savic, I (2013). Long-term occupational stress is associated with regional reductions in brain tissue volumes. PLOS ONE 8, e64065.Google Scholar
Cobia, DJ, Csernansky, JG, Wang, L (2011). Cortical thickness in neuropsychologically near-normal schizophrenia. Schizophrenia Research 133, 68–76.CrossRefGoogle ScholarPubMed
Cobia, DJ, Smith, MJ, Wang, L, Csernansky, JG (2012). Longitudinal progression of frontal and temporal lobe changes in schizophrenia. Schizophrenia Research 139, 1–6.Google Scholar
Crespo-Facorro, B, Perez-Iglesias, R, Mata, I, Martinez-Garcia, O, Ortiz, V, Pelayo-Teran, JM, Valdizan, E, Vazquez-Barquero, JL (2012). Long-term (3-year) effectiveness of haloperidol, risperidone and olanzapine: results of a randomized, flexible-dose, open-label comparison in first-episode nonaffective psychosis. Psychopharmacology (Berlin) 219, 225–233.Google Scholar
Crespo-Facorro, B, Roiz-Santianez, R, Perez-Iglesias, R, Rodriguez-Sanchez, JM, Mata, I, Tordesillas-Gutierrez, D, Sanchez, E, Tabares-Seisdedos, R, Andreasen, N, Magnotta, V, Vazquez-Barquero, JL (2011). Global and regional cortical thinning in first-episode psychosis patients: relationships with clinical and cognitive features. Psychological Medicine 41, 1449–1460.Google Scholar
Crespo-Facorro, B, Roiz-Santianez, R, Perez-Iglesias, R, Tordesillas-Gutierrez, D, Mata, I, Rodriguez-Sanchez, JM, de Lucas, EM, Vazquez-Barquero, JL (2009). Specific brain structural abnormalities in first-episode schizophrenia. A comparative study with patients with schizophreniform disorder, non-schizophrenic non-affective psychoses and healthy volunteers. Schizophrenia Research 115, 191–201.Google Scholar
DeLisi, LE (2008). The concept of progressive brain change in schizophrenia: implications for understanding schizophrenia. Schizophrenia Bulletin 34, 312–321.CrossRefGoogle ScholarPubMed
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, e45081.Google Scholar
Ehrlich, S, Brauns, S, Yendiki, A, Ho, BC, Calhoun, V, Schulz, SC, Gollub, RL, Sponheim, SR (2012). Associations of cortical thickness and cognition in patients with schizophrenia and healthy controls. Schizophrenia Bulletin 38, 1050–1062.CrossRefGoogle ScholarPubMed
Engvig, A, Fjell, AM, Westlye, LT, Moberget, T, Sundseth, O, Larsen, VA, Walhovd, KB (2010). Effects of memory training on cortical thickness in the elderly. NeuroImage 52, 1667–1676.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, J (2001). Structured Clinical Interview for DSM-IV-TR Axis I Disorders – Non-Patient Edition. New York State Psychiatric Institute: New York.Google Scholar
Fjell, AM, Walhovd, KB (2010). Structural brain changes in aging: courses, causes and cognitive consequences. Reviews in the Neurosciences 21, 187–221.CrossRefGoogle ScholarPubMed
Goghari, VM, Smith, GN, Honer, WG, Kopala, LC, Thornton, AE, Su, W, Macewan, GW, Lang, DJ (2013). Effects of eight weeks of atypical antipsychotic treatment on middle frontal thickness in drug-naive first-episode psychosis patients. Schizophrenia Research 149, 149–155.CrossRefGoogle ScholarPubMed
Grube, BS, Bilder, RM, Goldman, RS (1998). Meta-analysis of symptom factors in schizophrenia. Schizophrenia Research 31, 113–120.Google Scholar
Haier, RJ, Karama, S, Leyba, L, Jung, RE (2009). MRI assessment of cortical thickness and functional activity changes in adolescent girls following three months of practice on a visual–spatial task. BMC Research Notes 2, 174.Google Scholar
Harris, G, Andreasen, NC, Cizadlo, T, Bailey, JM, Bockholt, HJ, Magnotta, VA, Arndt, S (1999). Improving tissue classification in MRI: a three-dimensional multispectral discriminant analysis method with automated training class selection. Journal of Computer Assisted Tomography 23, 144–154.Google Scholar
Ho, BC, Alicata, D, Ward, J, Moser, DJ, O'Leary, DS, Arndt, S, Andreasen, NC (2003). Untreated initial psychosis: relation to cognitive deficits and brain morphology in first-episode schizophrenia. American Journal of Psychiatry 160, 142–148.Google Scholar
Horacek, J, Bubenikova-Valesova, V, Kopecek, M, Palenicek, T, Dockery, C, Mohr, P, Hoschl, C (2006). Mechanism of action of atypical antipsychotic drugs and the neurobiology of schizophrenia. CNS Drugs 20, 389–409.Google Scholar
Janca, A, Kastrup, M, Katschnig, H, Lopez-Ibor, JJ Jr, Mezzich, JE, Sartorius, N (1996). The World Health Organization Short Disability Assessment Schedule (WHO DAS-S): a tool for the assessment of difficulties in selected areas of functioning of patients with mental disorders. Social Psychiatry and Psychiatric Epidemiology 31, 349–354.Google Scholar
Keshavan, MS, Haas, GL, Kahn, CE, Aguilar, E, Dick, EL, Schooler, NR, Sweeney, JA, Pettegrew, JW (1998). Superior temporal gyrus and the course of early schizophrenia: progressive, static, or reversible? Journal of Psychiatric Research 32, 161–167.CrossRefGoogle ScholarPubMed
Kubota, M, Miyata, J, Yoshida, H, Hirao, K, Fujiwara, H, Kawada, R, Fujimoto, S, Tanaka, Y, Sasamoto, A, Sawamoto, N, Fukuyama, H, Murai, T (2011). Age-related cortical thinning in schizophrenia. Schizophrenia Research 125, 21–29.Google Scholar
Kuperberg, GR, Broome, MR, McGuire, PK, David, AS, Eddy, M, Ozawa, F, Goff, D, West, WC, Williams, SC, van der Kouwe, AJ, Salat, DH, Dale, AM, Fischl, B (2003). Regionally localized thinning of the cerebral cortex in schizophrenia. Archives of General Psychiatry 60, 878–888.Google Scholar
Lamont, AJ, Mortby, ME, Anstey, KJ, Sachdev, PS, Cherbuin, N (2014). Using sulcal and gyral measures of brain structure to investigate benefits of an active lifestyle. NeuroImage 91, 353–359.Google Scholar
Magnotta, VA, Harris, G, Andreasen, NC, O'Leary, DS, Yuh, WT, Heckel, D (2002). Structural MR image processing using the BRAINS2 toolbox. Computerized Medical Imaging and Graphics 26, 251–264.Google Scholar
Malla, AK, Bodnar, M, Joober, R, Lepage, M (2011). Duration of untreated psychosis is associated with orbital-frontal grey matter volume reductions in first episode psychosis. Schizophrenia Research 125, 13–20.Google Scholar
Menezes, NM, Arenovich, T, Zipursky, RB (2006). A systematic review of longitudinal outcome studies of first-episode psychosis. Psychological Medicine 36, 1349–1362.Google Scholar
Mondelli, V, Pariante, CM, Navari, S, Aas, M, D'Albenzio, A, Di Forti, M, Handley, R, Hepgul, N, Marques, TR, Taylor, H, Papadopoulos, AS, Aitchison, KJ, Murray, RM, Dazzan, P (2010). Higher cortisol levels are associated with smaller left hippocampal volume in first-episode psychosis. Schizophrenia Research 119, 75–78.Google Scholar
Mosconi, L, Murray, J, Tsui, WH, Li, Y, Davies, M, Williams, S, Pirraglia, E, Spector, N, Osorio, RS, Glodzik, L, McHugh, P, de Leon, MJ (2014). Mediterranean diet and magnetic resonance imaging-assessed brain atrophy in cognitively normal individuals at risk for Alzheimer's disease. Journal of Prevention of Alzheimer's Disease 1, 23–32.Google Scholar
Mueser, KT, McGurk, SR (2004). Schizophrenia. Lancet 363, 2063–2072.Google Scholar
Narr, KL, Bilder, RM, Toga, AW, Woods, RP, Rex, DE, Szeszko, PR, Robinson, D, Sevy, S, Gunduz-Bruce, H, Wang, YP, DeLuca, H, Thompson, PM (2005). Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cerebral Cortex 15, 708–719.Google Scholar
Nesvag, R, Bergmann, O, Rimol, LM, Lange, EH, Haukvik, UK, Hartberg, CB, Fagerberg, T, Soderman, E, Jonsson, EG, Agartz, I (2012). A 5-year follow-up study of brain cortical and subcortical abnormalities in a schizophrenia cohort. Schizophrenia Research 142, 209–216.CrossRefGoogle Scholar
Nesvag, R, Lawyer, G, Varnas, K, Fjell, AM, Walhovd, KB, Frigessi, A, Jonsson, EG, Agartz, I (2008). Regional thinning of the cerebral cortex in schizophrenia: effects of diagnosis, age and antipsychotic medication. Schizophrenia Research 98, 16–28.Google Scholar
Okugawa, G, Takase, K, Nobuhara, K, Yoshida, T, Minami, T, Tamagaki, C, Magnotta, VA, Andreasen, NC, Kinoshita, T (2003). Inter- and intraoperator reliability of brain tissue measures using magnetic resonance imaging. European Archives of Psychiatry and Clinical Neuroscience 253, 301–306.Google Scholar
Overall, JE, Gorman, DR (1962). The Brief Psychiatric Rating Scale. Psychological Reports 10, 799–812.Google Scholar
Pelayo-Teran, JM, Perez-Iglesias, R, Ramirez-Bonilla, M, Gonzalez-Blanch, C, Martinez-Garcia, O, Pardo-Garcia, G, Rodriguez-Sanchez, JM, Roiz-Santianez, R, Tordesillas-Gutierrez, D, Mata, I, Vazquez-Barquero, JL, Crespo-Facorro, B (2008). Epidemiological factors associated with treated incidence of first-episode non-affective psychosis in Cantabria: insights from the Clinical Programme on Early Phases of Psychosis. Early Intervention Psychiatry 2, 178–187.Google Scholar
Peters, A, Kemper, T (2012). A review of the structural alterations in the cerebral hemispheres of the aging rhesus monkey. Neurobiology of Aging 33, 2357–2372.Google Scholar
Rodríguez-Sánchez, JM, Ayesa-Arriola, R, Pérez-Iglesias, R, Periañez, JA, Martinez-Garcia, O, Gomez-Ruiz, E, Tabares-Seisdedos, R, Crespo-Facorro, B (2013). Course of cognitive deficits in first episode of non-affective psychosis: a 3-year follow-up study. Schizophrenia Research 150, 121–128.Google Scholar
Roiz-Santianez, R, Ayesa-Arriola, R, Tordesillas-Gutierrez, D, Ortiz-Garcia de la Foz, V, Perez-Iglesias, R, Pazos, A, Sanchez, E, Crespo-Facorro, B (2014). Three-year longitudinal population-based volumetric MRI study in first-episode schizophrenia spectrum patients. Psychological Medicine 44, 1591–1604.Google Scholar
Roiz-Santianez, R, Tordesillas-Gutierrez, D, Ortiz-Garcia de la Foz, V, Ayesa-Arriola, R, Gutierrez, A, Tabares-Seisdedos, R, Vazquez-Barquero, JL, Crespo-Facorro, B (2012). Effect of antipsychotic drugs on cortical thickness. A randomized controlled one-year follow-up study of haloperidol, risperidone and olanzapine. Schizophrenia Research 141, 22–28.Google Scholar
Savic, I (2013). Structural changes of the brain in relation to occupational stress. Cerebral Cortex. Published online 18 December 2013. doi:10.1093/cercor/bht348.Google ScholarPubMed
Schaufelberger, MS, Lappin, JM, Duran, FL, Rosa, PG, Uchida, RR, Santos, LC, Murray, RM, McGuire, PK, Scazufca, M, Menezes, PR, Busatto, GF (2011). Lack of progression of brain abnormalities in first-episode psychosis: a longitudinal magnetic resonance imaging study. Psychological Medicine 41, 1677–1689.Google Scholar
Schneider, CE, White, T, Hass, J, Geisler, D, Wallace, SR, Roessner, V, Holt, DJ, Calhoun, VD, Gollub, RL, Ehrlich, S (2014). Smoking status as a potential confounder in the study of brain structure in schizophrenia. Journal of Psychiatric Research 50, 84–91.CrossRefGoogle Scholar
Sizonenko, SV, Babiloni, C, Sijben, JW, Walhovd, KB (2013). Brain imaging and human nutrition: which measures to use in intervention studies? Advances in Nutrition 4, 554–556.Google Scholar
Steen, RG, Mull, C, McClure, R, Hamer, RM, Lieberman, JA (2006). Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. British Journal of Psychiatry 188, 510–518.CrossRefGoogle ScholarPubMed
Thompson, PM, Vidal, C, Giedd, JN, Gochman, P, Blumenthal, J, Nicolson, R, Toga, AW, Rapoport, JL (2001). Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proceedings of the National Academy of Sciences 98, 11650–11655.Google Scholar
Tuladhar, AM, Reid, AT, Shumskaya, E, de Laat, KF, van Norden, AG, van Dijk, EJ, Norris, DG, de Leeuw, FE (2015). Relationship between white matter hyperintensities, cortical thickness, and cognition. Stroke 46, 425–432.Google Scholar
Van Haren, NE, Cahn, W, Hulshoff Pol, HE, Kahn, RS (2013). Confounders of excessive brain volume loss in schizophrenia. Neuroscience and Biobehavioral Reviews 37, 2418–2423.Google Scholar
Van Haren, NE, Schnack, HG, Cahn, W, van den Heuvel, MP, Lepage, C, Collins, L, Evans, AC, Hulshoff Pol, HE, Kahn, RS (2011). Changes in cortical thickness during the course of illness in schizophrenia. Archives of General Psychiatry 68, 871–880.Google Scholar
Vita, A, De Peri, L, Deste, G, Barlati, S, Sacchetti, E (2015). The effect of antipsychotic treatment on cortical gray matter changes in schizophrenia: does the class matter? A meta-analysis and meta-regression of longitudinal magnetic resonance imaging studies. Biological Psychiatry. Published online 16 February 2015. doi:10.1016/j.biopsych.2015.02.008.Google Scholar
Zipursky, RB, Reilly, TJ, Murray, RM (2013). The myth of schizophrenia as a progressive brain disease. Schizophrenia Bulletin 39, 1363–1372.CrossRefGoogle ScholarPubMed
Supplementary material: File

Roiz-Santiáñez supplementary material

Tables S1-S4

Download Roiz-Santiáñez supplementary material(File)
File 32.3 KB