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Articles   |    
Neuropsychological Decline in Schizophrenia From the Premorbid to the Postonset Period: Evidence From a Population-Representative Longitudinal Study
Madeline H. Meier, Ph.D.; Avshalom Caspi, Ph.D.; Abraham Reichenberg, Ph.D.; Richard S.E. Keefe, Ph.D.; Helen L. Fisher, Ph.D.; HonaLee Harrington, B.S.; Renate Houts, Ph.D.; Richie Poulton, Ph.D.; Terrie E. Moffitt, Ph.D.
Am J Psychiatry 2014;171:91-101. doi:10.1176/appi.ajp.2013.12111438
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Dr. Keefe has received investigator-initiated research funding support from the Department of Veterans Affairs, Feinstein Institute for Medical Research, GlaxoSmithKline, NIMH, Novartis, Psychogenics, Research Foundation for Mental Hygiene, and Singapore National Medical Research Council; he has received honoraria from or served as a consultant or advisory board member for Abbott, Akebia, Amgen, Astellas, Asubio, BiolineRx, Biomarin, Boehringer-Ingelheim, Bristol-Myers Squibb, Eli Lilly, EnVivo, Helicon, Lundbeck, Merck, Mitsubishi, Novartis, Otsuka, Pfizer, Roche, Shire, Sunovion, Takeda, and Targacept; he receives royalties for the BACS testing battery and the MATRICS Battery (BACS Symbol Coding) and is a shareholder in NeuroCog Trials. The other authors report no financial relationships with commercial interests.

Supported in part by the National Institute on Aging (grant AG032282) and the U.K. Medical Research Council (grant MR/K00381X). The Dunedin Multidisciplinary Health and Development Research Unit is supported by the New Zealand Health Research Council. Dr. Meier was supported by National Institute on Drug Abuse grant P30 DA023026 and by the Jacobs Foundation.

From the Department of Psychology and Neuroscience, Duke University, Durham, N.C.; the Duke Transdisciplinary Prevention Research Center, Center for Child and Family Policy, Duke University, Durham; the Institute for Genome Sciences and Policy, Duke University, Durham; the Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham; the Department of Psychosis Studies and the Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry, King’s College London; and the Dunedin Multidisciplinary Health and Development Research Unit, Department of Preventive and Social Medicine, School of Medicine, University of Otago, Dunedin, New Zealand.

Address correspondence to Dr. Moffitt (terrie.moffitt@duke.edu).

Copyright © 2014 by the American Psychiatric Association

Received November 19, 2012; Revised April 14, 2013; Revised May 23, 2013; Accepted June 03, 2013.

Abstract

Objective  Despite the widespread belief that neuropsychological decline is a cardinal feature of the progression from the premorbid stage to the chronic form of schizophrenia, few longitudinal studies have examined change in neuropsychological functioning from before to after illness onset. The authors examined whether neuropsychological decline is unique to schizophrenia, whether it is generalized or confined to particular mental functions, and whether individuals with schizophrenia also have cognitive problems in everyday life.

Method  Participants were members of a representative cohort of 1,037 individuals born in Dunedin, New Zealand, in 1972 and 1973 and followed prospectively to age 38, with 95% retention. Assessment of IQ and specific neuropsychological functions was conducted at ages 7, 9, 11, and 13, and again at age 38. Informants also reported on any cognitive problems at age 38.

Results  Individuals with schizophrenia exhibited declines in IQ and in a range of mental functions, particularly those tapping processing speed, learning, executive function, and motor function. There was little evidence of decline in verbal abilities or delayed memory, however, and the developmental progression of deficits in schizophrenia differed across mental functions. Processing speed deficits increased gradually from childhood to beyond the early teen years, whereas verbal deficits emerged early but remained static thereafter. Neuropsychological decline was specific to schizophrenia, as no evidence of decline was apparent among individuals with persistent depression, children with mild cognitive impairment, individuals matched on childhood risk factors for schizophrenia, and psychiatrically healthy individuals. Informants also noticed more cognitive problems in individuals with schizophrenia.

Conclusions  There is substantial neuropsychological decline in schizophrenia from the premorbid to the postonset period, but the extent and developmental progression of decline varies across mental functions. Findings suggest that different pathophysiological mechanisms may underlie deficits in different mental functions.

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FIGURE 1. IQ in Childhood and Adulthood in Individuals With Schizophrenia, Persistent Depression, or Mild Cognitive Impairment and Healthy Comparison Subjectsa

a Panel A shows full-scale IQ in childhood (averaged across ages 7–13) and adulthood (age 38) for the healthy, schizophrenia, and persistent-depression groups. There was a statistically significant difference (paired t=3.29, p=0.003) between childhood and adulthood IQ for members of the schizophrenia group. Panel B shows full-scale IQ in childhood (ages 7, 9, 11, and 13) and adulthood (age 38) for the healthy, schizophrenia, and persistent-depression groups as well as a group of children with mild cognitive impairment. IQ was stable across childhood for all groups but declined for the schizophrenia group between ages 13 and 38. Error bars indicate standard error.

FIGURE 2. Scaled Scores on Subtests of the WISC-R and WAIS-IV IQ in Individuals With Schizophrenia, Persistent Depression, or Mild Cognitive Impairment and Healthy Comparison Subjectsa

a Panel A shows scaled scores (population mean=10.00, SD=3.00) on the Wechsler digit symbol coding subtest from age 7 to age 38. The deficit among individuals with schizophrenia increased from ages 7 to 38. Panel B shows scaled scores (population mean=10.00, SD = 3.00) on the Wechsler similarities subtest from age 7 to age 38. The deficit among individuals with schizophrenia was apparent as early as age 7 and remained relatively stable from age 7 to age 38. Error bars indicate standard error.

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TABLE 1.Characteristics of Studies Assessing Neuropsychological Decline From Before to After the Onset of Schizophreniaa
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a Studies are ordered by methodology and date, with the most methodologically rigorous and recent studies listed first. The first two studies (11, 12) used epidemiological samples; all the others used clinical samples.

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b The same test was used across time within participants, but not between participants.

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TABLE 2.Comparison of Cohort Members Diagnosed With Schizophrenia Who Had or Had Not Received Treatment for Psychotic Illness
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a Ns varied because of different amounts of missing data across study measures.

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b Based on self-report.

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c Standardized to cohort (mean=0.00, SD=1.00).

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TABLE 3.Mean Scores on Childhood Risk Factors for Cohort Members Who Did (Case) or Did Not (Control) Develop Schizophrenia, Before and After Propensity Score Matchinga
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a We used propensity score matching to perform the match using SAS (SAS, Inc., Cary, N.C.). First, we obtained propensity scores via a logistic regression predicting likelihood of developing schizophrenia based on the childhood correlates listed here. Next, we performed an optimal 2-to-1 (control-to-case) match on these propensity scores, whereby matches were made on the basis of the absolute difference in propensity score between case and control subjects. The maximum absolute difference was set to 0.10. Results were similar across models with different match parameters (i.e., varied number of case subjects matched to control subjects, varied maximum absolute difference). A total of 906 study members (31 case subjects and 875 control subjects) were available for matching, as analyses required nonmissing values for all childhood risk factors. The table shows that matching resulted in a high degree of similarity in the distributions of the childhood risk factors across case and control subjects, as standardized bias after matching was below 10 for each risk factor. Negative standardized bias values indicate higher risk in the control group.

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b Standardized to cohort (mean=0.00, SD=1.00).

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TABLE 4.Neuropsychological Decline Across Different Mental Functions in Individuals With Schizophrenia or Persistent Depression and Healthy Comparison Subjectsa
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a The table lists mean childhood and adulthood neuropsychological test scores (in standard deviation units) for each group. The change column (Δ) indicates the change in test scores (in standard deviation units) from childhood to adulthood. Statistical tests are adjusted for sex. Ns for the IQ subtests range from 514 to 518 for the healthy group, 30 to 31 for the schizophrenia group, and 184 to 185 for the persistent depression group. A subset of cohort members completed IQ testing in childhood but did not complete the Rey Auditory Verbal Learning Test, the Trail Making Test (parts A and B), or the Grooved Pegboard Test in childhood; for these tests, the Ns are 384–393 for the healthy group, 21–22 for the schizophrenia group, and 138–140 for the persistent depression group. There were no significant differences in IQ decline between those who completed these tests and those who did not, either for the cohort as a whole or for the healthy, schizophrenia, or persistent depression groups.

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b Significant difference (p<0.05) compared with the healthy group.

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c Higher scores on these tests indicate worse performance. Positive change scores on these tests reflect decline in performance from childhood to adulthood.

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TABLE 5.Ruling Out Alternative Explanations for the Observed Neuropsychological Decline in Schizophreniaa
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a Mean change in IQ from childhood to adulthood is listed in standard deviation units. Statistical tests compare each psychiatric group to the healthy group and are adjusted for sex.

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TABLE 6.Cognitive Impairment in Everyday Life in Individuals With Schizophrenia or Persistent Depression and Healthy Comparison Subjectsa
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a Age-38 informant-reported attention and memory problem ratings are listed in standard deviation units. Statistical tests compare each psychiatric group to the healthy group and are adjusted for sex.

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