Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-06T10:57:13.521Z Has data issue: false hasContentIssue false
  • English
  • Français

A population-based longitudinal study of childhood neurodevelopmental disorders, IQ and subsequent risk of psychotic experiences in adolescence

Published online by Cambridge University Press:  25 April 2014

G. M. Khandaker ,
J. Stochl ,
S. Zammit ,
G. Lewis  and
P. B. Jones
G. M. Khandaker*
Affiliation:
Department of Psychiatry, University of Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK Centre for Mental Health, Addiction and Suicide Research, School of Social and Community Medicine, University of Bristol, UK
J. Stochl
Affiliation:
Department of Psychiatry, University of Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK
S. Zammit
Affiliation:
Centre for Mental Health, Addiction and Suicide Research, School of Social and Community Medicine, University of Bristol, UK Institute of Psychological Medicine and Clinical Neurosciences, MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University, UK
G. Lewis
Affiliation:
Centre for Mental Health, Addiction and Suicide Research, School of Social and Community Medicine, University of Bristol, UK Mental Health Sciences Unit, University College London, UK
P. B. Jones
Affiliation:
Department of Psychiatry, University of Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK
*
*Address for correspondence: Dr G. M. Khandaker, Department of Psychiatry, Box 189, Cambridge Biomedical Campus, Cambridge CB2 2QQ, UK. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background.

Schizophrenia has a neurodevelopmental component to its origin, and may share overlapping pathogenic mechanisms with childhood neurodevelopmental disorders (NDs). Nevertheless, longitudinal studies of psychotic outcomes among individuals with NDs are limited. We report a population-based prospective study of six common childhood NDs, subsequent neurocognitive performance and the risk of psychotic experiences (PEs) in early adolescence.

Method.

PEs were assessed by semi-structured interviews at age 13 years. IQ and working memory were measured between ages 9 and 11 years. The presence of six NDs (autism spectrum, dyslexia, dyspraxia, dysgraphia, dysorthographia, dyscalculia) was determined from parent-completed questionnaires at age 9 years. Linear regression calculated the mean difference in cognitive scores between children with and without NDs. Associations between NDs and PEs were expressed as odds ratios (ORs) with 95% confidence intervals (CIs); effects of cognitive deficits were examined. Potential confounders included age, gender, father's social class, ethnicity and maternal education.

Results.

Out of 8220 children, 487 (5.9%) were reported to have NDs at age 9 years. Children with, compared with those without, NDs performed worse on all cognitive measures; the adjusted mean difference in total IQ was 6.84 (95% CI 5.00–8.69). The association between total IQ and NDs was linear (p < 0.0001). The risk of PEs was higher in those with, compared with those without, NDs; the adjusted OR for definite PEs was 1.76 (95% CI 1.11–2.79). IQ (but not working memory) deficit partly explained this association.

Conclusions.

Higher risk of PEs in early adolescence among individuals with childhood ND is consistent with the neurodevelopmental hypothesis of schizophrenia.

Keywords

autism spectrum disorderdyslexiaIQneurocognitive performanceneurodevelopmental disorderpsychotic experiences
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 15 , November 2014 , pp. 3229 - 3238
Copyright
Copyright © Cambridge University Press 2014 

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

Aylward, E, Walker, E, Bettes, B (1984). Intelligence in schizophrenia: meta-analysis of the research. Schizophrenia Bulletin 10, 430–459.CrossRefGoogle ScholarPubMed
Baron, RM, Kenny, DA (1986). The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology 51, 1173–1182.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Scott, FJ, Allison, C, Williams, J, Bolton, P, Matthews, FE, Brayne, C (2009). Prevalence of autism-spectrum conditions: UK school-based population study. British Journal of Psychiatry 194, 500–509.CrossRefGoogle ScholarPubMed
Bassett, AS, Scherer, SW, Brzustowicz, LM (2010). Copy number variations in schizophrenia: critical review and new perspectives on concepts of genetics and disease. American Journal of Psychiatry 167, 899–914.CrossRefGoogle ScholarPubMed
Bevan, Jones R, Thapar, A, Lewis, G, Zammit, S (2012). The association between early autistic traits and psychotic experiences in adolescence. Schizophrenia Research 135, 164–169.Google Scholar
Boyd, A, Golding, J, Macleod, J, Lawlor, DA, Fraser, A, Henderson, J, Molloy, L, Ness, A, Ring, S, Davey, Smith G (2013). Cohort Profile: the ‘children of the 90s’ – the index offspring of the Avon Longitudinal Study of Parents and Children. International Journal of Epidemiology 42, 111–127.Google Scholar
Butterworth, B, Reigosa, V (2007). Information processing deficits in dyscalculia. In Why Is Math So Hard for Some Children? The Nature and Origins of Mathematical Learning Difficulties and Disabilities (ed. Berch, D and Mazzocco, M), pp. 65–81. Paul H. Brookes Publishing: Baltimore, MD.Google Scholar
Cannon, M, Caspi, A, Moffitt, TE, Harrington, H, Taylor, A, Murray, RM, Poulton, R (2002). Evidence for early-childhood, pan-developmental impairment specific to schizophreniform disorder: results from a longitudinal birth cohort. Archives of General Psychiatry 59, 449–456.Google Scholar
Cannon, TD, Bearden, CE, Hollister, JM, Rosso, IM, Sanchez, LE, Hadley, T (2000). Childhood cognitive functioning in schizophrenia patients and their unaffected siblings: a prospective cohort study. Schizophrenia Bulletin 26, 379–393.Google Scholar
Case, R, Kurland, DM, Goldberg, J (1982). Operational efficiency and the growth of short-term memory span. Journal of Experimental Child Psychology 33, 386–404.Google Scholar
Crow, TJ, Done, DJ, Sacker, A (1995). Childhood precursors of psychosis as clues to its evolutionary origins. European Archives of Psychiatry and Clinical Neuroscience 245, 61–69.CrossRefGoogle ScholarPubMed
De Loore, E, Gunther, N, Drukker, M, Feron, F, Sabbe, B, Deboutte, D, van Os, J, Myin-Germeys, I (2011). Persistence and outcome of auditory hallucinations in adolescence: a longitudinal general population study of 1800 individuals. Schizophrenia Research 127, 252–256.Google Scholar
Finch, AJ, Chihldress, WB (1975). A comparison of WISC selected subtest short forms with MR children. Mental Retardation 13, 20–21.Google Scholar
Fraser, A, Macdonald-Wallis, C, Tilling, K, Boyd, A, Golding, J, Davey, Smith G, Henderson, J, Macleod, J, Molloy, L, Ness, A, Ring, S, Nelson, SM, Lawlor, DA (2013). Cohort Profile: the Avon Longitudinal Study of Parents and Children: ALSPAC mothers cohort. International Journal of Epidemiology 42, 97–110.Google Scholar
Gold, JM, Goldberg, RW, McNary, SW, Dixon, LB, Lehman, AF (2002). Cognitive correlates of job tenure among patients with severe mental illness. American Journal of Psychiatry 159, 1395–1402.Google Scholar
Horwood, J, Salvi, G, Thomas, K, Duffy, L, Gunnell, D, Hollis, C, Lewis, G, Menezes, P, Thompson, A, Wolke, D, Zammit, S, Harrison, G (2008). IQ and non-clinical psychotic symptoms in 12-year-olds: results from the ALSPAC birth cohort. British Journal of Psychiatry 193, 185–191.Google Scholar
Howes, OD, Shotbolt, P, Bloomfield, M, Daalman, K, Demjaha, A, Diederen, KM, Ibrahim, K, Kim, E, McGuire, P, Kahn, RS, Sommer, IE (2013). Dopaminergic function in the psychosis spectrum: an [18F]-DOPA imaging study in healthy individuals with auditory hallucinations. Schizophrenia Bulletin 39, 807–814.Google Scholar
Hulme, C, Snowling, MJ (2009). Developmental Disorders of Language, Learning and Cognition. Wiley-Blackwell: Chichester, UK.Google Scholar
Hutton, J, Goode, S, Murphy, M, Le Couteur, A, Rutter, M (2008). New-onset psychiatric disorders in individuals with autism. Autism 12, 373–390.CrossRefGoogle ScholarPubMed
Jones, P, Rodgers, B, Murray, R, Marmot, M (1994). Child development risk factors for adult schizophrenia in the British 1946 birth cohort. Lancet 344, 1398–1402.Google Scholar
Kelleher, I, Cannon, M (2011). Psychotic-like experiences in the general population: characterizing a high-risk group for psychosis. Psychological Medicine 41, 1–6.Google Scholar
Khandaker, GM, Barnett, JH, White, IR, Jones, PB (2011). A quantitative meta-analysis of population-based studies of premorbid intelligence and schizophrenia. Schizophrenia Research 132, 220–227.CrossRefGoogle ScholarPubMed
Khandaker, GM, Zammit, S, Lewis, G, Jones, PB (2014). A population-based study of atopic disorders and inflammatory markers in childhood before psychotic experiences in adolescence. Schizophrenia Research 152, 139–145.CrossRefGoogle ScholarPubMed
Kirov, G, Rujescu, D, Ingason, A, Collier, DA, O'Donovan, MC, Owen, MJ (2009). Neurexin 1 (NRXN1) deletions in schizophrenia. Schizophrenia Bulletin 35, 851–854.Google Scholar
Matson, JL, Shoemaker, M (2009). Intellectual disability and its relationship to autism spectrum disorders. Research in Developmental Disabilities 30, 1107–1114.CrossRefGoogle ScholarPubMed
Murray, GK, Jones, PB (2012). Psychotic symptoms in young people without psychotic illness: mechanisms and meaning. British Journal of Psychiatry 201, 4–6.Google Scholar
Murray, RM, Lewis, SW (1987). Is schizophrenia a neurodevelopmental disorder? British Medical Journal (Clinical Research Edition) 295, 681–682.Google Scholar
Muthen, LK, Muthen, BO (1998–2014). MPlus User's Guide, Seventh Edition. Los Angeles, CA: Muthen & Muthen.Google Scholar
Niarchou, M, Zammit, S, Walters, J, Lewis, G, Owen, MJ, van den Bree, MB (2013). Defective processing speed and nonclinical psychotic experiences in children: longitudinal analyses in a large birth cohort. American Journal of Psychiatry 170, 550–557.Google Scholar
Owen, MJ, O'Donovan, MC, Thapar, A, Craddock, N (2011). Neurodevelopmental hypothesis of schizophrenia. British Journal of Psychiatry 198, 173–175.CrossRefGoogle ScholarPubMed
Polanczyk, G, Moffitt, TE, Arseneault, L, Cannon, M, Ambler, A, Keefe, RS, Houts, R, Odgers, CL, Caspi, A (2010). Etiological and clinical features of childhood psychotic symptoms: results from a birth cohort. Archives of General Psychiatry 67, 328–338.Google Scholar
Poulton, R, Caspi, A, Moffitt, TE, Cannon, M, Murray, R, Harrington, H (2000). Children's self-reported psychotic symptoms and adult schizophreniform disorder: a 15-year longitudinal study. Archives of General Psychiatry 57, 1053–1058.Google Scholar
Rai, D, Lewis, G, Lundberg, M, Araya, R, Svensson, A, Dalman, C, Carpenter, P, Magnusson, C (2012). Parental socioeconomic status and risk of offspring autism spectrum disorders in a Swedish population-based study. Journal of the American Academy of Child and Adolescent Psychiatry 51, 467–476. e6.Google Scholar
Rajji, TK, Ismail, Z, Mulsant, BH (2009). Age at onset and cognition in schizophrenia: meta-analysis. British Journal of Psychiatry 195, 286–293.CrossRefGoogle ScholarPubMed
Rapoport, J, Chavez, A, Greenstein, D, Addington, A, Gogtay, N (2009). Autism spectrum disorders and childhood-onset schizophrenia: clinical and biological contributions to a relation revisited. Journal of the American Academy of Child and Adolescent Psychiatry 48, 10–18.Google Scholar
Richardson, AJ, Ross, MA (2000). Fatty acid metabolism in neurodevelopmental disorder: a new perspective on associations between attention-deficit/hyperactivity disorder, dyslexia, dyspraxia and the autistic spectrum. Prostaglandins, Leukotrienes and Essential Fatty Acids 63, 1–9.CrossRefGoogle ScholarPubMed
Rubio, JM, Sanjuan, J, Florez-Salamanca, L, Cuesta, MJ (2012). Examining the course of hallucinatory experiences in children and adolescents: a systematic review. Schizophrenia Research 138, 248–254.Google Scholar
Scalais, E, Nuttin, C, Galluzzo, A (2005). Developmental dyspraxia. In Current Management in Child Neurology (ed. Maria, B. L.), pp. 240–245. BC Decker Inc.: Ontario, Canada.Google Scholar
Shaffer, D, Fisher, P, Lucas, CP, Dulcan, MK, Schwab-Stone, ME (2000). NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child and Adolescent Psychiatry 39, 28–38.Google Scholar
Stricker, G, Merbaum, M, Tangeman, P (1968). WAIS short forms, information transmission and approximation of full scale IQ. Journal of Clinical Psychology 25, 170–172.3.0.CO;2-L>CrossRefGoogle Scholar
Sullivan, PF, Magnusson, C, Reichenberg, A, Boman, M, Dalman, C, Davidson, M, Fruchter, E, Hultman, CM, Lundberg, M, Langstrom, N, Weiser, M, Svensson, AC, Lichtenstein, P (2012). Family history of schizophrenia and bipolar disorder as risk factors for autism. Archives of General Psychiatry 69, 1099–1103.Google Scholar
Sullivan, S, Rai, D, Golding, J, Zammit, S, Steer, C (2013). The association between autism spectrum disorder and psychotic experiences in the Avon Longitudinal Study of Parents and Children (ALSPAC) birth cohort. Journal of the American Academy of Child and Adolescent Psychiatry 52, 806–814.Google Scholar
Thomas, K, Harrison, G, Zammit, S, Lewis, G, Horwood, J, Heron, J, Hollis, C, Wolke, D, Thompson, A, Gunnell, D (2009). Association of measures of fetal and childhood growth with non-clinical psychotic symptoms in 12-year-olds: the ALSPAC cohort. British Journal of Psychiatry 194, 521–526.Google Scholar
Thomas, P, Zahorodny, W, Peng, B, Kim, S, Jani, N, Halperin, W, Brimacombe, M (2012). The association of autism diagnosis with socioeconomic status. Autism 16, 201–213.Google Scholar
Unenge, Hallerback M, Lugnegard, T, Gillberg, C (2012). Is autism spectrum disorder common in schizophrenia? Psychiatry Research 198, 12–17.CrossRefGoogle Scholar
van Os, J, Linscott, RJ, Myin-Germeys, I, Delespaul, P, Krabbendam, L (2009). A systematic review and meta-analysis of the psychosis continuum: evidence for a psychosis proneness-persistence-impairment model of psychotic disorder. Psychological Medicine 39, 179–195.Google Scholar
Vernes, SC, Newbury, DF, Abrahams, BS, Winchester, L, Nicod, J, Groszer, M, Alarcon, M, Oliver, PL, Davies, KE, Geschwind, DH, Monaco, AP, Fisher, SE (2008). A functional genetic link between distinct developmental language disorders. New England Journal of Medicine 359, 2337–2345.CrossRefGoogle ScholarPubMed
Wechsler, D, Golombok, S, Rust, J (1992). Weschler Intelligence Scale for Children, 3rd UK Edition (WISC-III UK). The Psychological Corporation: New York, NY.Google Scholar
Weinberger, DR (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 44, 660–669.Google Scholar
WHO (1994). SCAN: Schedules for Clinical Assessment in Neuropsychiatry, Version 2.0. World Health Organization: Geneva.Google Scholar
Williams, NM, Zaharieva, I, Martin, A, Langley, K, Mantripragada, K, Fossdal, R, Stefansson, H, Stefansson, K, Magnusson, P, Gudmundsson, OO, Gustafsson, O, Holmans, P, Owen, MJ, O'Donovan, M, Thapar, A (2010). Rare chromosomal deletions and duplications in attention-deficit hyperactivity disorder: a genome-wide analysis. Lancet 376, 1401–1408.Google Scholar
Wing, L (1980). Childhood autism and social class: a question of selection? British Journal of Psychiatry 137, 410–417.Google Scholar
Zammit, S, Kounali, D, Cannon, M, David, AS, Gunnell, D, Heron, J, Jones, PB, Lewis, S, Sullivan, S, Wolke, D, Lewis, G (2013). Psychotic experiences and psychotic disorders at age 18 in relation to psychotic experiences at age 12 in a longitudinal population-based cohort study. American Journal of Psychiatry 170, 742–750.Google Scholar
Zammit, S, Odd, D, Horwood, J, Thompson, A, Thomas, K, Menezes, P, Gunnell, D, Hollis, C, Wolke, D, Lewis, G, Harrison, G (2009). Investigating whether adverse prenatal and perinatal events are associated with non-clinical psychotic symptoms at age 12 years in the ALSPAC birth cohort. Psychological Medicine 39, 1457–1467.Google Scholar
Supplementary material: File

Khandaker Supplementary Material

Supplementary Material

Download Khandaker Supplementary Material(File)
File 20.7 KB