Caudate nucleus volume in medicated and unmedicated patients with early- and adult-onset schizophrenia.

Humans Caudate Nucleus / diagnostic imaging Schizophrenia / drug therapy Adult Female Male Antipsychotic Agents / therapeutic use Adolescent Age of Onset Magnetic Resonance Imaging Young Adult Organ Size / drug effects Case-Control Studies
Adult-onset Antipsychotics Caudate Early-onset MRI Schizophrenia

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
01 Oct 2024
Historique:
received: 20 03 2024
accepted: 16 09 2024
medline: 2 10 2024
pubmed: 2 10 2024
entrez: 1 10 2024
Statut: epublish

Résumé

The caudate nucleus is a part of the striatum, and striatal hyperdopaminergia is considered central to the pathophysiology of schizophrenia. How caudate volume is affected in schizophrenia and what role antipsychotics play remains unclear. In early-onset schizophrenia (EOS), where psychosis emerges during a neurodevelopmentally critical phase, the caudate may exhibit a heightened vulnerability to the effects of antipsychotic medications. We hypothesized effects of both antipsychotic medication use and age of onset on caudate in schizophrenia. We included adult patients with EOS (n = 83) and adult-onset schizophrenia (AOS) (n = 246), adult healthy controls (HC, n = 774), adolescent patients with non-affective psychosis (n = 56) and adolescent HC (n = 97). We obtained T1-weighted MRI scans using a 1.5T Siemens scanner and General Electric 3T scanners. In our main analysis, we tested for main and interaction effects of diagnosis and current antipsychotic medication use on caudate volume. Adult patients with EOS (p < 0.001) and AOS (p = 0.002) had both larger caudate than HC. Age of onset (EOS/AOS) interacted with antipsychotic use (p = 0.004) which was associated with larger caudate in EOS (p < 0.001) but not in AOS (p = 0.654). Conversely, among medicated patients only, EOS had larger caudate than AOS (p < 0.001). No other subcortical structures showed differences between medicated EOS and AOS. Medicated adolescent patients with non-affective psychosis and medicated adult patients with EOS showed similar caudate volumes. The results may indicate a schizophrenia-related and a medication-induced caudate increase, the latter restricted to patients with EOS and possibly occurring already in adolescence shortly after disease onset.

Identifiants

DOI: 10.1038/s41598-024-73322-x PMID: 39353988
pubmed: 39353988
doi: 10.1038/s41598-024-73322-x
pii: 10.1038/s41598-024-73322-x
doi:

Substances chimiques

Antipsychotic Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

22755

Informations de copyright

© 2024. The Author(s).

Références

Salomon, J. A. et al. Common values in assessing health outcomes from disease and injury: Disability weights measurement study for the Global Burden of Disease Study 2010. Lancet380, 2129–2143. https://doi.org/10.1016/S0140-6736(12)61680-8 (2012).
doi: 10.1016/S0140-6736(12)61680-8 pubmed: 23245605 pmcid: 10782811
Kahn, R. S. et al. Schizophrenia. Nat. Rev. Dis. Primers1, 15067. https://doi.org/10.1038/nrdp.2015.67 (2015).
doi: 10.1038/nrdp.2015.67 pubmed: 27189524
Clemmensen, L., Vernal, D. L. & Steinhausen, H. C. A systematic review of the long-term outcome of early onset schizophrenia. BMC Psychiatry12, 150. https://doi.org/10.1186/1471-244X-12-150 (2012).
doi: 10.1186/1471-244X-12-150 pubmed: 22992395 pmcid: 3521197
Diaz-Caneja, C. M. et al. Predictors of outcome in early-onset psychosis: A systematic review. NPJ. Schizophr.1, 14005. https://doi.org/10.1038/npjschz.2014.5 (2015).
doi: 10.1038/npjschz.2014.5 pubmed: 27336027 pmcid: 4849440
Perez-Costas, E., Melendez-Ferro, M. & Roberts, R. C. Basal ganglia pathology in schizophrenia: Dopamine connections and anomalies. J. Neurochem.113, 287–302. https://doi.org/10.1111/j.1471-4159.2010.06604.x (2010).
doi: 10.1111/j.1471-4159.2010.06604.x pubmed: 20089137 pmcid: 2929831
Brisch, R. et al. The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: old fashioned, but still in vogue. Front. Psychiatry5, 47. https://doi.org/10.3389/fpsyt.2014.00047 (2014).
doi: 10.3389/fpsyt.2014.00047 pubmed: 24904434 pmcid: 4032934
Howes, O. D. & Kapur, S. The dopamine hypothesis of schizophrenia: Version III–the final common pathway. Schizophr. Bull.35, 549–562. https://doi.org/10.1093/schbul/sbp006 (2009).
doi: 10.1093/schbul/sbp006 pubmed: 19325164 pmcid: 2669582
Davis, K. L., Kahn, R. S., Ko, G. & Davidson, M. Dopamine in schizophrenia: A review and reconceptualization. Am. J. Psychiatry148, 1474–1486. https://doi.org/10.1176/ajp.148.11.1474 (1991).
doi: 10.1176/ajp.148.11.1474 pubmed: 1681750
Chen, S. Y. et al. Parcellation of the striatal complex into dorsal and ventral districts. Proc. Natl. Acad. Sci. U. S. A.117, 7418–7429. https://doi.org/10.1073/pnas.1921007117 (2020).
doi: 10.1073/pnas.1921007117 pubmed: 32170006 pmcid: 7132256
Grahn, J. A., Parkinson, J. A. & Owen, A. M. The cognitive functions of the caudate nucleus. Prog. Neurobiol.86, 141–155. https://doi.org/10.1016/j.pneurobio.2008.09.004 (2008).
doi: 10.1016/j.pneurobio.2008.09.004 pubmed: 18824075
Klein, M. O. et al. Dopamine: Functions, signaling, and association with neurological diseases. Cell Mol. Neurobiol.39, 31–59. https://doi.org/10.1007/s10571-018-0632-3 (2019).
doi: 10.1007/s10571-018-0632-3 pubmed: 30446950
Gurholt, T. P. et al. Intracranial and subcortical volumes in adolescents with early-onset psychosis: A multisite mega-analysis from the ENIGMA consortium. Hum. Brain Mapp.43, 373–384. https://doi.org/10.1002/hbm.25212 (2022).
doi: 10.1002/hbm.25212 pubmed: 33017498
Haijma, S. V. et al. Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophr. Bull.39, 1129–1138. https://doi.org/10.1093/schbul/sbs118 (2013).
doi: 10.1093/schbul/sbs118 pubmed: 23042112
van Erp, T. G. et al. Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Mol. Psychiatry21, 547–553. https://doi.org/10.1038/mp.2015.63 (2016).
doi: 10.1038/mp.2015.63 pubmed: 26033243
Okada, N. et al. Abnormal asymmetries in subcortical brain volume in schizophrenia. Mol. Psychiatry21, 1460–1466. https://doi.org/10.1038/mp.2015.209 (2016).
doi: 10.1038/mp.2015.209 pubmed: 26782053 pmcid: 5030462
Fusar-Poli, P. et al. Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neurosci. Biobehav. Rev.37, 1680–1691. https://doi.org/10.1016/j.neubiorev.2013.06.001 (2013).
doi: 10.1016/j.neubiorev.2013.06.001 pubmed: 23769814 pmcid: 3964856
Chakos, M. H. et al. Striatal enlargement in rats chronically treated with neuroleptic. Biol. Psychiatry44, 675–684. https://doi.org/10.1016/s0006-3223(98)00029-8 (1998).
doi: 10.1016/s0006-3223(98)00029-8 pubmed: 9798070
Vernon, A. C. et al. Contrasting effects of haloperidol and lithium on rodent brain structure: A magnetic resonance imaging study with postmortem confirmation. Biol. Psychiatry71, 855–863. https://doi.org/10.1016/j.biopsych.2011.12.004 (2012).
doi: 10.1016/j.biopsych.2011.12.004 pubmed: 22244831
Wang, Y., Xu, Q., Luo, J., Hu, M. & Zuo, C. Effects of age and sex on subcortical volumes. Front. Aging Neurosci.11, 259. https://doi.org/10.3389/fnagi.2019.00259 (2019).
doi: 10.3389/fnagi.2019.00259 pubmed: 31616285 pmcid: 6775221
Lenroot, R. K. et al. Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage36, 1065–1073. https://doi.org/10.1016/j.neuroimage.2007.03.053 (2007).
doi: 10.1016/j.neuroimage.2007.03.053 pubmed: 17513132
Arain, M. et al. Maturation of the adolescent brain. Neuropsychiatr. Dis. Treat.9, 449–461. https://doi.org/10.2147/NDT.S39776 (2013).
doi: 10.2147/NDT.S39776 pubmed: 23579318 pmcid: 3621648
Franca, T. F. A. & Pompeia, S. Reappraising the role of dopamine in adolescent risk-taking behavior. Neurosci. Biobehav. Rev.147, 105085. https://doi.org/10.1016/j.neubiorev.2023.105085 (2023).
doi: 10.1016/j.neubiorev.2023.105085 pubmed: 36773751
Wahlstrom, D., White, T. & Luciana, M. Neurobehavioral evidence for changes in dopamine system activity during adolescence. Neurosci. Biobehav. Rev.34, 631–648. https://doi.org/10.1016/j.neubiorev.2009.12.007 (2010).
doi: 10.1016/j.neubiorev.2009.12.007 pubmed: 20026110
Teicher, M. H., Andersen, S. L. & Hostetter, J. C. Jr. Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Brain Res. Dev. Brain Res.89, 167–172. https://doi.org/10.1016/0165-3806(95)00109-q (1995).
doi: 10.1016/0165-3806(95)00109-q pubmed: 8612321
Dwyer, J. B. & Leslie, F. M. Adolescent maturation of dopamine D1 and D2 receptor function and interactions in rodents. PLoS One11, e0146966. https://doi.org/10.1371/journal.pone.0146966 (2016).
doi: 10.1371/journal.pone.0146966 pubmed: 26784516 pmcid: 4718668
Lin, W. C., Delevich, K. & Wilbrecht, L. A role for adaptive developmental plasticity in learning and decision making. Curr. Opin. Behav. Sci.36, 48–54. https://doi.org/10.1016/j.cobeha.2020.07.010 (2020).
doi: 10.1016/j.cobeha.2020.07.010 pubmed: 35891805 pmcid: 9311400
Wiley, J. L. Antipsychotic-induced suppression of locomotion in juvenile, adolescent and adult rats. Eur. J. Pharmacol.578, 216–221. https://doi.org/10.1016/j.ejphar.2007.09.010 (2008).
doi: 10.1016/j.ejphar.2007.09.010 pubmed: 17935710
Stevens, R. M., Gannon, M. A., Griffith, M. S. & Bardgett, M. E. Delayed yet persistent effects of daily risperidone on activity in developing rats. Behav. Pharmacol.27, 460–469. https://doi.org/10.1097/FBP.0000000000000230 (2016).
doi: 10.1097/FBP.0000000000000230 pubmed: 26960160 pmcid: 4935566
First, M. B., Spitzer, R. L., Gibbon, M. & Williams, J. B. Structured Clinical inTERVIEw for DSM-IV Axis I Disorders (SCIDI), Clinician Version, Administration Booklet (American Psychiatric Association Publishing, 2012).
Spitzer, R. L. et al. Utility of a new procedure for diagnosing mental disorders in primary care. The PRIME-MD 1000 study. JAMA272, 1749–1756 (1994).
doi: 10.1001/jama.1994.03520220043029 pubmed: 7966923
Kaufman, J. et al. Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data. J. Am. Acad. Child Adolesc. Psychiatry36, 980–988. https://doi.org/10.1097/00004583-199707000-00021 (1997).
doi: 10.1097/00004583-199707000-00021 pubmed: 9204677
Werry, J. S., McClellan, J. M. & Chard, L. Childhood and adolescent schizophrenic, bipolar, and schizoaffective disorders: a clinical and outcome study. J. Am. Acad. Child Adolesc. Psychiatry30, 457–465. https://doi.org/10.1097/00004583-199105000-00017 (1991).
doi: 10.1097/00004583-199105000-00017 pubmed: 2055884
Kay, S. R., Fiszbein, A. & Opler, L. A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull.13, 261–276. https://doi.org/10.1093/schbul/13.2.261 (1987).
doi: 10.1093/schbul/13.2.261 pubmed: 3616518
Andreasen, N. C., Pressler, M., Nopoulos, P., Miller, D. & Ho, B. C. Antipsychotic dose equivalents and dose-years: A standardized method for comparing exposure to different drugs. Biol. Psychiatry67, 255–262. https://doi.org/10.1016/j.biopsych.2009.08.040 (2010).
doi: 10.1016/j.biopsych.2009.08.040 pubmed: 19897178
Bohn, M. J., Babor, T. F. & Kranzler, H. R. The alcohol use disorders identification test (AUDIT): Validation of a screening instrument for use in medical settings. J. Stud. Alcohol.56, 423–432. https://doi.org/10.15288/jsa.1995.56.423 (1995).
doi: 10.15288/jsa.1995.56.423 pubmed: 7674678
Berman, A. H., Bergman, H., Palmstierna, T. & Schlyter, F. Evaluation of the drug use disorders identification test (DUDIT) in criminal justice and detoxification settings and in a Swedish population sample. Eur. Addict. Res.11, 22–31. https://doi.org/10.1159/000081413 (2005).
doi: 10.1159/000081413 pubmed: 15608468
Fischl, B. FreeSurfer. Neuroimage62, 774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021 (2012).
doi: 10.1016/j.neuroimage.2012.01.021 pubmed: 22248573
Haddad, E. et al. Multisite test-retest reliability and compatibility of brain metrics derived from FreeSurfer versions 71, 60, and 53. Hum. Brain Mapp.44, 1515–1532. https://doi.org/10.1002/hbm.26147 (2023).
doi: 10.1002/hbm.26147 pubmed: 36437735
Perlaki, G. et al. Comparison of accuracy between FSL’s FIRST and freesurfer for caudate nucleus and putamen segmentation. Sci. Rep.7, 2418. https://doi.org/10.1038/s41598-017-02584-5 (2017).
doi: 10.1038/s41598-017-02584-5 pubmed: 28546533 pmcid: 5445091
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Statist. Soc. B57, 289–300 (1995).
doi: 10.1111/j.2517-6161.1995.tb02031.x
Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t-tests and ANOVAs. Front. Psychol.4, 863. https://doi.org/10.3389/fpsyg.2013.00863 (2013).
doi: 10.3389/fpsyg.2013.00863 pubmed: 24324449 pmcid: 3840331
Lawrie, S. M. et al. Brain structure, genetic liability, and psychotic symptoms in subjects at high risk of developing schizophrenia. Biol. Psychiatry49, 811–823. https://doi.org/10.1016/s0006-3223(00)01117-3 (2001).
doi: 10.1016/s0006-3223(00)01117-3 pubmed: 11343678
Hannan, K. L. et al. Caudate nucleus volume in individuals at ultra-high risk of psychosis: A cross-sectional magnetic resonance imaging study. Psychiatry Res.182, 223–230. https://doi.org/10.1016/j.pscychresns.2010.02.006 (2010).
doi: 10.1016/j.pscychresns.2010.02.006 pubmed: 20488675
Mamah, D. et al. Basal ganglia shape abnormalities in the unaffected siblings of schizophrenia patients. Biol. Psychiatry64, 111–120. https://doi.org/10.1016/j.biopsych.2008.01.004 (2008).
doi: 10.1016/j.biopsych.2008.01.004 pubmed: 18295189 pmcid: 2486271
Rajarethinam, R., Upadhyaya, A., Tsou, P., Upadhyaya, M. & Keshavan, M. S. Caudate volume in offspring of patients with schizophrenia. Br. J. Psychiatry191, 258–259. https://doi.org/10.1192/bjp.bp.106.029017 (2007).
doi: 10.1192/bjp.bp.106.029017 pubmed: 17766768
Andersen, H. G. et al. Striatal volume increase after six weeks of selective dopamine D2/3 receptor blockade in first-episode, Antipsychotic-Naive Schizophrenia Patients. Front. Neurosci.14, 484. https://doi.org/10.3389/fnins.2020.00484 (2020).
doi: 10.3389/fnins.2020.00484 pubmed: 32508577 pmcid: 7251943

Auteurs

Dimitrios Andreou (D)

Department of Psychiatric Research, Diakonhjemmet Hospital, Forskningsveien 7, 0373, Oslo, Norway. dimitrios.andreou@ki.se.
Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway. dimitrios.andreou@ki.se.
Centre for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet & Stockholm Health Care Services, Stockholm Region, Stockholm, Sweden. dimitrios.andreou@ki.se.

Kjetil Nordbø Jørgensen (KN)

Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Division of Mental Health and Addiction, Vestre Viken Hospital Trust, Drammen, Norway.

Stener Nerland (S)

Department of Psychiatric Research, Diakonhjemmet Hospital, Forskningsveien 7, 0373, Oslo, Norway.
Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Tereza Calkova (T)

Centre for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet & Stockholm Health Care Services, Stockholm Region, Stockholm, Sweden.
Centre for Clinical Research, Vastmanland Hospital Vasteras, Region Vastmanland - Uppsala University, Västerås, Sweden.

Lynn Mørch-Johnsen (L)

Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Department of Psychiatry, Department of Clinical Research, Østfold Hospital, Grålum, Norway.

Runar Elle Smelror (RE)

Department of Psychiatric Research, Diakonhjemmet Hospital, Forskningsveien 7, 0373, Oslo, Norway.
Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Laura A Wortinger (LA)

Department of Psychiatric Research, Diakonhjemmet Hospital, Forskningsveien 7, 0373, Oslo, Norway.
Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Mathias Lundberg (M)

Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden.

Hannes Bohman (H)

Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden.
Department of Neuroscience, Child and Adolescent Psychiatry and Psychiatry Unit, Uppsala University, Uppsala, Sweden.

Anne Margrethe Myhre (AM)

Division of Mental Health and Addiction, Departement of Research and innovation, Oslo University Hospital, Oslo, Norway.
Child and Adolescent Psychiatry Unit, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Erik G Jönsson (EG)

Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Centre for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet & Stockholm Health Care Services, Stockholm Region, Stockholm, Sweden.

Ole A Andreassen (OA)

Division of Mental Health and Addiction, Norwegian Centre for Mental Disorders Research (NORMENT), Oslo University Hospital, Oslo, Norway.

Ingrid Agartz (I)

Department of Psychiatric Research, Diakonhjemmet Hospital, Forskningsveien 7, 0373, Oslo, Norway.
Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Centre for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet & Stockholm Health Care Services, Stockholm Region, Stockholm, Sweden.

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