Download Are Communication Deviance and Expressed Emotion Related to

Are Communication Deviance and Expressed
Emotion Related to Family History of
Psychiatric Disorders in Schizophrenia?
by Kenneth L. Subotnik, Michael J. Qoldstein, Keith H. Nuechterlein,
Stephanie M. Woo, and Jim Mint?
(2) affective attitudes and behaviors expressed toward
another family member, usually one who has manifested
some signs of a psychiatric disorder. The work of Wynne
and Singer provides the best operational criteria for disturbed communicational processes, which they termed
communication deviance (CD; Wynne and Singer 1963a,
1963£; Wynne et al. 1977). Note that the CD measure
identifies not psychiatric deviance but specific aspects of
communication style. The most heavily researched construct related to affective attitude is expressed emotion
(EE; Brown et al. 1972), defined as notable attitudes of
criticism and/or emotional overinvolvement manifested in
a semistructured interview, the Camberwell Family Interview (CFI; Brown and Rutter 1966).
A major assumption underlying this line of research,
particularly in the case of biological parents of young
adult schizophrenia patients, has been that these measures
reflect ongoing family transactions that are stressors for
persons who are in regular contact with high-CD or highEE relatives (Nuechterlein et al. 1989; Miklowitz and
Stackman 1992; Hooley and Gotlib 2000). There are other
possible explanations of their apparent clinical significance. For example, these attributes may represent indirect
assessments of a major psychiatric disorder in the parent.
That question has been studied. The results have been
largely, although not entirely, negative. A previous report
(Goldstein et al. 1992) on a sample of 56 parents of 41
recent-onset schizophrenia patients found that high CD in
relatives was not related to the presence of either a past or
a present psychiatric disorder. Negative findings were also
obtained for the CFI-EE assessment. The Five-Minute
Speech Sample Method (FMSS-EE; Magafia et al. 1986)
did suggest that relatives with a lifetime diagnosis of a
severe psychiatric disorder were more likely to have high
FMSS-EE, and that tendency was even stronger using a
composite index based on both the CFI- and FMSS-EE
measures, which were separated by a 4- to 5-week period.
Abstract
Studies have reported that certain measures of intrafamilial transactions are associated with an increased
risk both for the initial onset of schizophrenia and for
its recurrence following the initial episode of disorder.
Two of the most studied of these are communication
deviance (CD), a measure of subclinical thought disorder expressed in speech, and expressed emotion (EE),
defined as notable attitudes of criticism and/or emotional overinvolvement manifested in a semistructured
interview. A previous study (Goldstein et al. 1992)
examined whether these two measures were associated
with the presence of a diagnosable psychiatric disorder
in the biological parents of recent-onset schizophrenia
patients. In general, they were not. The present study
went one step further. It examined whether these same
measures were correlated with family history of schizophrenia or affective disorder in the biological parents
and siblings of these same parents. High EE was not
associated with a greater family history of schizophrenia spectrum disorders among the parent's parents
and siblings but was unexpectedly found to be
inversely associated with familial affective disorders.
In contrast, CD was associated with a family history of
schizophrenia spectrum disorders among the parent's
parents and siblings. The findings are consistent with
the possibility that CD may be an indicator of a
genetic vulnerability factor for schizophrenia.
Keywords: Schizophrenia, thought disorder, family study, communication deviance, expressed emotion,
vulnerability indicator, family environment.
Schizophrenia Bulletin, 28(4):719-729, 2002.
Certain measures of intrafamilial transactions have been
consistently associated with an increased risk for recurrence of schizophrenic psychosis following the initial
episode of the disorder (see Goldstein 1987, and Hooley
and Hiller 2001, for reviews of these findings). Two attributes that have been studied extensively are (1) the clarity
of communication between parents and their offspring and
Send reprint requests to Dr. K. L. Subotnik, Department of Psychiatry
and Biobehavioral Sciences, University of California, Los Angeles, 300
UCLA Medical Plaza, Room 2240, Los Angeles, CA 90095-6968; email: [email protected].
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Schizophrenia Bulletin, Vol. 28, No. 4, 2002
K.L. Subotnik et al.
The present study took this line of research one step
further to consider whether our previous findings were
generally negative because, by virtue of their parenthood
status, these relatives would be unlikely to have a severe
psychiatric disorder such as schizophrenia (Gottesman
1991). Therefore, we decided to examine the question of
whether CD and even EE tap a predisposition to a psychiatric disorder that is not clinically expressed. If these measures were found to be related to a family history of a
schizophrenia-related disorder among the subject's parents
and siblings, this would be consistent with a familially
transmitted predispositional factor for schizophrenia,
which other evidence suggests is primarily genetic in origin (Kendler 2000). Some evidence supportive of this view
has recently been presented by Docherty et al. (19996) for
another index of communication disturbance. Therefore,
we examined whether high levels of EE or CD were
related to a family history of schizophrenia spectrum disorders in the parents and siblings of the biological parents
of individuals with schizophrenia. A contrast measure of a
family history of affective disorder was also examined in
relation to EE and CD.
Methods
Subjects. The current study involved linkage of data
from three separate protocols, each of which contributed
data in some form to the current analyses. These protocols
involved separate informed consent procedures, different
research measures, and different inclusion criteria.
Contributing Project 1: Developmental Processes
in Schizophrenic Disorders (principal investigator
[PI]: K.H.N.). The main protocol was the first one within
the Developmental Processes in Schizophrenic Disorders
project, a longitudinal prospective study of the early
course of schizophrenia in young adult patients
(Nuechterlein et al. 1992). This project followed 104
patients with a recent onset of schizophrenia. As part of
the initial protocol, Developmental Processes in Outcome,
significant others with whom the patients had at least
weekly contact were asked to participate in a research
interview, the CFI (Vaughn and Leff 1976), to assess EE
(CFI-EE). At least one biological parent in 67 families, for
a total of 105 parent-subjects, participated.
Because the biological parents of the patients, not the
patients themselves, were the subjects in the present study,
the patient sample will be described only briefly here. A
complete description of the selection criteria for the
patient sample can be found in Nuechterlein et al. (1992).
All patients were required to have a diagnosis of schizophrenia or schizoaffective disorder, mainly schizophrenic,
by Research Diagnostic Criteria (RDC; Spitzer et al.
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1978), with the patient's first psychotic episode occurring
less than 2 years prior to project contact. An active psychotic period of at least 2 weeks was required. The
patients were screened and selected from consecutive
admissions to four local public psychiatric hospitals and
referrals to the University of California, Los Angeles
(UCLA) Adult Psychiatry outpatient department. Family
history of psychiatric illness was not considered in patient
selection. Patients with current significant and habitual
drug and alcohol abuse, or with a history of abuse that
made the diagnosis of schizophrenia ambiguous, were
excluded. At the time of entry into the study, the mean age
of the 67 patients was 23.2 years (standard deviation [SD]
= 4.6, range 18 to 44 years); the mean years of school was
12.5 (SD = 1.8, range 8 to 16 years); and 57 patients (85%)
were male, 10 were female. Sixty patients were non-Hispanic Caucasian, 3 were Hispanic, 1 was Asian, and 3
were of mixed racial background.
Contributing Project 2: Coping Behavior in
Schizophrenia (UCLA Family Project; PI: M.J.G.).
Approximately 4 to 5 weeks after the patients began outpatient treatment as part of Project 1, the parents were
asked to participate in a second, separate protocol to
assess family attitudes and interactions. A total of 94 biological parents participated in Project 2. A measure of
subclinical thought disorder (i.e., CD) administered at the
UCLA Family Project was used for this report.
Contributing Project 3: The UCLA Family Study
(PI: K.H.N.). The third protocol was a family study of
psychiatric disorders and neurocognitive vulnerability factors. At least 1 biological family member from 79 of the
104 families of the Developmental Processes in Outcome
patients participated. Of the 158 biological parents of
patients in these 79 families, 111 were interviewed in person. Of those parents not directly interviewed (n - Al), 25
(10 mothers and 15 fathers) were deceased, 7 (2 mothers
and 5 fathers) lived far from Los Angeles and were not
available to be interviewed, 5 (fathers) could not be
located, and 10 (3 mothers and 7 fathers) declined to be
interviewed. Thus, of the 121 living parents who were
located, lived locally, and were contacted by the research
team, 92 percent were directly interviewed.
Demographics of parents. Ninety-eight parent-subjects (60 mothers and 38 fathers) participated in both
Project 1 and Project 3. These parent-subjects were an
average of 55 years old at the time of the Family Study
assessment (SD = 7.5). They had a mean of 13.9 years of
education (SD = 2.8) and a mean socioeconomic status of
2.9 (SD = 1.2) (Hollingshead 1957). Eighty-six parentsubjects were Caucasian, 6 were Hispanic, 2 were AfricanAmerican, 2 were Asian, and 2 were of mixed racial background. Somewhat fewer (89) parent-subjects participated
in both Project 2 and Project 3. These 89 subjects were
Communication Deviance and Expressed Emotion
Schizophrenia Bulletin, Vol. 28, No. 4, 2002
demographically similar to the 98 participants in both
Project 1 and Project 3. The 98 parent-subjects in the current report include the 56 originally described in the prior
report of the relationship of CD and EE to the personal
psychiatric history of the parents (Goldstein et al. 1992).
study, it involved only a subgroup of parents who chose to
participate (a separate informed consent process and form
were completed). The staff who collected these diagnostic
data had no overlap with those who collected the EE and
CD data.
The first part of the Family Study involved face-toface diagnostic interviews with the parent. Clinical psychiatric syndromes were assessed with the Diagnostic Interview Schedule (DIS; Robins et al. 1981), with
supplemental questions regarding psychotic symptoms
selected from the Present State Exam (PSE; Wing et al.
1974); the supplemental questions were asked if there was
evidence of the symptoms. The presence of any of five
selected personality disorders (schizotypal, paranoid,
schizoid, avoidant, and borderline) was assessed using the
Structured Clinical Interview for DSM-HI-R (SCID-II;
Spitzer et al. 1987). Extensive followup questions were
asked if indicated by the subject's response to the initial
probe question for any individual criterion.
Following this interview concerning personal history
of psychiatric disorders, each parent then participated in a
family history interview that covered psychiatric disorders
in the first and second degree relatives, plus the cousins, of
the schizophrenia patient. All family history diagnoses
were based on symptoms reported by the interviewee and
did not rely on the interviewee's memory of what diagnoses had been given to the family members. This history
was collected using the Relative Psychiatric History format developed by Gershon (1985). Diagnosis for the noninterviewed second and third degree relatives was made
using the Family History Research Diagnostic Criteria
(Andreasen et al. 1977). Personality disorder symptoms
were assessed with the SCID-II, which we adapted for a
family history interview format as follows. Initial screening questions were used to assess for the presence of personality disorder symptoms in the subject's first and second degree relatives. If there was evidence of personality
pathology relevant to one or more of the five personality
disorders examined here, the SCID-II questions for these
disorders were asked in the third person. Standard
DSM-III-R (American Psychiatric Association 1987) criteria were used to rate personality disorder diagnoses.
When family history information on these relatives was
also available from the subject's spouse, a consensus diagnosis was made from these sources.
The Family Study interviewers had clinical training in
psychiatric diagnosis and had substantial experience conducting structured diagnostic interviews. Training in the
use of the modified DIS/PSE involved didactic instruction,
co-rating taped interviews, and live interviews (Fogelson
et al. 1991; Subotnik et al. 1997). David Fogelson, M.D.,
trained the staff to administer the SCID-II and family history interview through a three-step procedure involving (1)
Procedures
Procedures from Project 1. As described above, the CFI
(Vaughn and Leff 1976) was administered to parent-subjects to assess EE as part of the Developmental Processes
study. The CFI was administered within a month of the
patient's index hospital admission or soon thereafter.
Procedures from Project 2. After discharge from the
hospital, the patients and the adult relatives with whom
they had at least weekly contact were informed of the separate study, Coping Behavior in Schizophrenia, in which
other family assessment data were collected. If they
agreed to participate, which required a separate informed
consent process and form, they were scheduled for a session approximately 4 to 5 weeks after the patient was discharged. A seven-card version of the Thematic
Apperception Test (TAT) was individually administered to
each subject to assess CD. The instructions requested that
the subject make up a story for each card covering what
led up to the scene portrayed in the picture, what was
occurring in the picture, how the characters were thinking
or feeling, and how the story might end. The subjects' stories were audiotaped, converted to transcripts, and scored
according to a 27-category system based on the original
Wynne-Singer system for operationalizing the construct
of CD as modified by Jones (1977) for the TAT. The TATCD system results in a mean z score representing the 27
categories weighted by their frequency relative to the
length of the total speech record, and expressed in SD
units based on previously collected normative data. In
addition, six factor scores are available from these data
based on the original work of Jones (1977); these scores
define specific clusters of the ways that CD can be manifested in the respondents' stories. The interrater reliability
(intraclass correlation) for the mean z score was 0.99 (p <
0.0001). The average intraclass correlation for the six factors was 0.90 (range 0.82 to 0.98, p < 0.001 for each;
Miklowitz et al. 1986, 1991). All coders of CFI-EE and
TAT-CD were blind to the diagnostic data that were collected subsequently from the parents of the schizophrenia
patients. Also, separate teams of raters made the CFI and
TAT-CD ratings, and each team operated without the
knowledge of the other's data.
Procedures from Project 3. Because the UCLA Family
Study was separate from the Developmental Processes
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K.L. Subotnik et al.
Schizophrenia Bulletin, Vol. 28, No. 4, 2002
may have contained individuals with other psychiatric disorders that were not examined in relation to the family
interaction variables under study.
having staff rate sample interviews conducted by Dr.
Fogelson with feedback from him on their symptom ratings and diagnoses; (2) administering practice interviews
with other staff and the trainer; and (3) administering the
modified DIS/PSE, SCID-II, and family history interview
to at least five subjects drawn from the adult inpatient service at the UCLA Neuropsychiatric Hospital and a temporary employment agency. Interviewers were considered to
have completed training when there was at least 90 percent agreement between their symptom ratings and the ratings of Dr. Fogelson. Ongoing weekly supervision was
provided to prevent drift in rating standards over time.
Reasonable reliability for assessing personality disorder
symptom dimensions using the SCID-II was established
based on 45 cases (intraclass correlations were 0.82 for
borderline, 0.73 for schizotypal, 0.70 for paranoid, 0.60
for schizoid, and 0.84 for avoidant; Fogelson et al. 1991).
The diagnoses that were generated for schizophrenia,
schizophrenia-related psychoses, and schizophrenia spectrum personality disorders using the family history
method were previously shown to have excellent specificity and positive predictive value but low sensitivity
(Fogelson et al., in press).
Following the collection of family history data, the
family history of each biological parent of a patient was
characterized by the presence of schizophrenia spectrum
disorders and affective disorders in the parent-subject's
own parents or siblings. This family history characterization excludes the offspring of these parent-subjects to
avoid confounding the genetic loading of mothers and
fathers within the same family. Although having such a
family history of schizophrenia spectrum disorders in siblings or parents does not formally represent obligate carrier status, it might be considered a proxy for such a carrier status, given that all parent-subjects had at least one
offspring with schizophrenia. If any parent or sibling of a
parent had a diagnosis of RDC schizophrenia, RDC
schizoaffective disorder, mainly schizophrenia, or
DSM-IJI-R schizotypal or paranoid personality disorder,
that parent-subject was classified as meeting this proxy
criteria for schizophrenia liability carrier status. This was
true for 14 (14.3%) of the family histories of the 98 parents who participated in both Projects 1 and 3. If any parent or sibling of a parent-subject satisfied criteria for RDC
schizoaffective disorder, mainly affective, RDC manic disorder, or RDC major depressive disorder, the parent-subject was classified as having an affective disorder familial
liability. This was true for 21 (21.4%) of the family histories of the 98 parents who participated in Projects 1 and 3,
with 5 of these 21 parent-subjects also meeting proxy criteria for schizophrenia spectrum disorder liability carrier
status. Sixty-eight parents had none of the above diagnoses in their parents or siblings. Note that those families
Data Analyses
The statistical model for the analysis of CD (a continuous and unimodally distributed variable) was a general
linear mixed model (SAS PROC MIXED). Family history among the parent-subject's own parents and siblings ("positive," "negative") and parent-subject gender
(i.e., mother, father) were fixed design effects in a 2 X 2
crossed design. Personal lifetime psychiatric history
(presence of any psychiatric disorder1) was included as a
covariate. Random family and error effects (assumed to
be independent) modeled possible nonindependence
within families (in fact, within-family correlation was
trivial, accounting for no more than 1% of the variance
in any analysis). The presence or absence of any of the
assessed personal RDC or DSM-III-R disorders was
entered as a covariate so that variance associated with
personal psychiatric pathology would be accounted for
statistically. The dichotomous EE variable was analyzed
with the same design, using the Generalized Estimating
Equation (GEE) approach of Liang and Zeger (1986).
The GEE analyses specified a logit link function, binomial error, and the exchangeable correlation structure (in
fact, any specification of the correlation structure would
produce the same results in this model because there was
only one covariance to model with a maximum of two
measures per family). The GEE program reports separate robust t tests for each of the fixed parameter estimates. Significant interactions of family history by parent status were followed up with analyses for each
parent separately, using simple contingency tables and
chi-square tests of significance. Separate analyses were
conducted for family history (among parents and siblings) of schizophrenia spectrum disorders and affective
disorders.
Results
CFI-EE. CFI-EE data from Project 1 were available for
98 of the subjects (60 mothers and 38 fathers) who also
participated in Project 3. Fifty-two participants (53%)
'Twenty-six mothers (43.3%) had one or more of the following lifetime personal psychiatric diagnoses: RDC schizophrenia; schizoaffective, manic, or major depressive disorder; DSM-III-R generalized anxiety disorder, or DSM-III-R avoidant. paranoid, schizotypal, schizoid, or
borderline personality disorder. Similarly, 16 fathers (42.1%) had one or
more of these psychiatric diagnoses.
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Schizophrenia Bulletin, Vol. 28, No. 4, 2002
CD. CD data from Project 2 were available for 89 of the
participants (53 mothers and 36 fathers) from Project 3.
For the main dependent measure, TAT-CD z score, there
was a statistically significant interaction between a family
history of schizophrenia spectrum disorder among the
subject's parents and siblings and parent gender (F = 4.06,
df = 1,58, p = 0.049). The statistical association between a
family history of schizophrenia spectrum disorder and CD
was observed among mothers (r = 2.54, df= 58, p < 0.02)
but not fathers (f = -0.85, df= 58, p = 0.40). Mothers with
a family history of schizophrenia spectrum disorders
among their parents and siblings had higher (i.e., worse)
TAT-CD z scores (n = 11, mean = 0.39, SD = 0.52) than
mothers with no such family history {n = 42, mean = 0.05,
SD = 0.35; table 2). Personal history of any lifetime psychiatric disorder accounted for very little of the variance
in TAT-CD z scores (t = 0.47, df = 58, p = 0.64) in the
overall analysis (both F < 1 in the separate analyses by
parent). Similar results were found when personal psychi-
were rated as high EE. The presence of a schizophrenia
spectrum disorder among the subject's parents and siblings was not associated with CFI-EE status of the parent
(main effect: z = 0.86, p = 0.39; interaction of family history X parent: z = -0.32, p = 0.75). However, there was a
statistically significant interaction of affective disorder
familial liability by parent gender (z = -2.22, p < 0.03).
Analyses done separately by parent gender revealed an
association for mothers (x 2 (l) = 5.95, p < 0.02) but not
fathers (x 2 (l) = 0.30, p = 0.58) (table 1). Mothers who
had a family history of affective disorders among their
own parents and siblings were more likely to be classified
as showing low rather than high CFI-EE attitudes. Only 2
of the 11 (18%) mothers with a family history of affective
disorder among their own parents and siblings were rated
as showing high CFI-EE attitudes, whereas 30 of 49
(61%) mothers with no affective disorder family history
among their parents and siblings were rated as having
high CFI-EE attitudes.
Table 1. Family history by CFI-EE status of 60 mothers and 38 fathers
CFI-EE Status
Mothers
Family history of schizophrenia
spectrum disorders1
Present
Absent
Test statistics
Family history of affective
disorders2
Present
Absent
Test statistics
Low
High
4
24
7
25
X 2 =0.30,
9
19
Fathers
Family history of schizophrenia
spectrum disorders1
Present
Absent
Test statistics
Family history of affective
disorders2
Present
Absent
Test statistics
df=-\,ns
X2=5.95, df=1,p<0.02 3 ' 4
2
30
2
18
1
17
X 2 = 0 . 2 6 , df=1,
ns
6
14
4
14
X 2 = 0.30, df =1,
Note.—CFI-EE = Camberwell Family Interview, expressed emotion; ns = nonsignificant; RDC = Research Diagnostic Criteria.
The schizophrenia spectrum disorders category is present if the parent has at least one parent or sibling with RDC schizophrenia, RDC
schizoaffective disorder, mainly schizophrenic, or DSM-III-R schizotypal or paranoid personality disorders.
2
The affective disorders category is present if the parent has at least one parent or sibling with a major depressive disorder, RDC bipolaraffective disorder, or RDC schizoaffective disorder, mainly affective.
3
Chi-square values are from the SAS Generalized Estimating Equation procedure with personal lifetime psychiatric history included as a
covariate. See Data Analyses section for details.
4
The simple 2 x 2 chi square for family history of affective disorders and CFI-EE status was x 2 = 6.69, <#= 1, p < 0.01.
1
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K.L. Subotnik et al.
Table 2. Family history of lifetime psychiatric diagnoses byTAT-CD mean z scores for 53 mothers and
36 fathers
TAT-CD z(SD)
Mothers
Fathers
Family history of schizophrenia spectrum disorders1
Present
0.39(0.52), n= 11
Absent
0.05 (0.35), n = 42
Test statistics
t=2.54, df= 58, p<0.02 2
0.15(0.44), n = 4
-0.03(0.31), n = 32
f = 0.85, df= 33, ns
Family history of affective disorders3
Present
Absent
Test statistics
-0.01 (0.35), /?= 10
0.19(0.45), n = 26
f = 1.27, df= 35, ns
0.06(0.62), n= 11
0.14(0.35), n = 42
f = -0.54, df = 58, ns
Note.—ns = nonsignificant; RDC = Research Diagnostic Criteria; SD = standard deviation; TAT-CD = Thematic Apperception Test, communication deviance.
1
The schizophrenia spectrum disorders category is present if the parent has at least one parent or sibling with RDC schizophrenia, RDC
schizoaffective disorder, mainly schizophrenic, or DSM-III-R schizotypal or paranoid personality disorders.
2
t test values are from the SAS general linear mixed model with personal lifetime psychiatric history as a covariate. See Data Analyses
section for details.
3
The affective disorders category is present if the parent has at least one parent or sibling with a major depressive disorder, RDC bipolaraffective disorder, or RDC schizoaffective disorder, mainly affective.
atric history was limited to the presence or absence of
schizophrenia spectrum disorders (i.e., RDC schizophrenia, RDC schizoaffective disorder, mainly schizophrenia,
or DSM-III-R schizotypal or paranoid personality disorder). There were no significant relationships between any
of the six CD factors and family history of schizophrenia
spectrum in the subjects' siblings or parents (p values for
the main effect of family history ranged from 0.65 to 0.96,
median = 0.86; for the interaction of family history by
parent gender from 0.10 to 0.92, median = 0.44). No significant relationship was found between family history of
affective disorder among the subjects' parents and siblings
and the subjects' TAT-CD z scores.
history. A genetic basis for the observed relationship is
possible but cannot be either confirmed or ruled out based
on this family study. An environment explanation of this
relationship might be that prior exposure to a severely
depressed relative may ameliorate somewhat the tendency
to be critical of one's own psychiatrically ill child and may
promote the development of more tolerant attitudes.
One might wonder why prior exposure to a family
member with an affective disorder, but not prior exposure
to a schizophrenia-related disorder, is associated with
lower EE attitudes toward an offspring with schizophrenia.
Several aspects need consideration. As we have pointed
out elsewhere, EE is likely to arise in the difficult context
in which relatives of schizophrenia patients struggle to
find ways of relating to their relative with severe mental
disorder (Miklowitz et al. 1989; Strachan et al. 1989;
Rosenfarb et al. 1995, 2000; Woo et al. 1997). Schizophrenia-related disorders are more likely than depressive disorders to involve a sustained family burden due to specific
disturbed behaviors and social performance deficits, which
have been found to be associated with high-EE attitudes
(Jackson et al. 1990). Thus, sustained exposure to schizophrenia may not lead as commonly to development of tolerant attitudes toward major psychiatric disorders. Previous exposure to a family member who experienced one or
more depressive episodes from which recovery occurred
without persistent disturbed behaviors and functional
impairment, on the other hand, may result in more hopeful
and tolerant attitudes when an offspring later develops a
psychiatric disorder.
The picture for CD looks quite different. The mean
across all 27 CD items (standardized) was positively asso-
Discussion
EE level of parents was not related to the degree of their
familial liability to schizophrenia spectrum disorders. This
is consistent with the general belief that EE does not
reflect a subclinical schizophrenia spectrum disorder. This
suggests that the oft-replicated finding that high-EE
parental status predicts higher relapse rates for patients
with schizophrenia cannot be accounted for by another
known prognostic variable: a family history of schizophrenia spectrum disorders.
We found that familial affective disorder (among parents and siblings of the parent-subjects) was associated
with reduced rather than increased likelihood of manifesting high-EE attitudes. A direct comparison to a previous
literature is not possible because no prior studies have
directly examined EE in relationship to family psychiatric
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Schizophrenia Bulletin, Vol. 28, No. 4, 2002
ciated with presence of a family history of schizophrenia
spectrum disorder in the respondent's parents and siblings,
albeit only on the maternal side. Scores on this measure
were not associated with a personal psychiatric diagnosis
in these parents. Separate analyses of the six CD factor
scores did not point to any specific component of CD, suggesting that it was overall CD that was related to maternal
family history.
This pattern in a family pedigree—the presence of
schizophrenia spectrum disorder in either the parents or
siblings of an individual, notable levels of CD in that individual, and schizophrenia in the individual's offspring
(i.e., the patient)—is genetically interpretable. The parent
of the patient in this situation is the probable carrier of
some psychosis-predisposing gene or genes. CD in such
biological parents of a schizophrenia patient might serve
as a subclinical indicator of a genetic predisposition to
psychotic disorder.
The notion that CD may be a subtle manifestation of a
genetic vulnerability to schizophrenia would be further
supported if CD was also related to neurocognitive deficits
in first degree relatives that are putative indicators of vulnerability factors for schizophrenia (Nuechterlein and
Dawson 1984; Asarnow et al. 1991; Braff 1993). Wagener
and colleagues found relationships within biological parents of schizophrenia patients between CD and performance on the Continuous Performance Test (CPT) and the
Span of Apprehension (SPAN) test (Wagener et al. 1986).
We have similarly found that some parental CD factor
scores in the current sample are significantly associated
with those parents' own CPT and SPAN performance
(Subotnik et al. 1999). However, a relationship between
neurocognitive measures and communication disturbance
in parents of schizophrenia patients has not consistently
been found (Docherty and Gordinier 1999).
We found that the association between parental CD
levels and presence of schizophrenia spectrum disorder in
parents and siblings of these parents was significant for
mothers, but not fathers, of schizophrenia patients. This
raises the question of gender effects. There is some evidence that family morbid risk for schizophrenia may be
higher among female than male schizophrenia patients
(Goldstein 1995), and DeLisi and Crow (1989) raised the
possibility of a sex-linked transmission pattern. Our data
cannot definitively tell us whether the observed relationship truly holds only for mothers, for several reasons.
First, the rate of participation of fathers was lower than for
mothers, limiting statistical power for fathers. Although
the data for fathers were in the same direction as for mothers, only four of the fathers had a parent or sibling with a
schizophrenia spectrum disorder. Second, we believe that
the fathers were not as knowledgeable as historians about
psychiatric disorders in their family members as were the
mothers. This would have decreased our sensitivity to
detect psychiatric disorders in the father's parents and siblings.
The finding that a subtle form of thought disorder is
associated with a familial history of schizophrenia spectrum disorders is consistent with the findings of Docherty
et al. (1999fo) for another index of communication abnormalities, the Communication Disturbances Index (CDI),
and a family history of psychotic disorders. CDI in parents
of schizophrenia patients was significantly associated with
a family history of psychotic disorders. While, by the simplest genetic view, one would expect that CDI in parents
would be directly associated with CDI in their offspring
with schizophrenia, Docherty et al. (1999a) found that this
was not the case. Instead, CDI scores in parents were associated with overall symptom severity in their offspring
with schizophrenia. However, Shenton et al. (1989) did
find such a parent-offspring correlation using the
Rorschach Thought Disorder Index. Thus, whether there is
a straightforward parent-offspring similarity in subtle
thought disorder levels remains unclear and may depend
on the measure of thought disorder that is used.
An alternative to the genetic view regarding influences on CD might be that CD, at least in part, is a result
of exposure to an immediate family member with schizophrenia spectrum disorder (Miklowitz and Stackman
1992). Prior studies of environmental effects have focused
almost exclusively on the possible impact of parent CD on
offspring schizophrenia spectrum disorder. However, there
is some evidence that contact with one's offspring with
schizophrenia might lead to disordered communication in
the parent (Liem 1974).
The complex interplay between genetic and environmental influences on thought disorder is seen in an intriguing study of adopted-away offspring of mothers with
schizophrenia (Wahlberg et al. 1997a, 19976). Their findings suggest that exposure to parental CD might potentiate
a genetic predisposition to schizophrenia. They reported
an interaction between having a biological parent with
schizophrenia and environmental exposure to a thoughtdisordered adoptive parent. Offspring with a biological
parent who had schizophrenia were more likely to develop
thought disorder when reared by adoptive parents with
high, as compared to low, CD. Offspring without a biological parent with schizophrenia were unlikely to develop
thought disorder regardless of the adoptive parents' levels
of CD.
One possible concern is the representativeness of the
current sample. The mean educational level of the subset
of 98 parents (13.9 years ± 2.8 SD) in this report seems
high, but it is not significantly different from the mean
educational level of all parents of the 104 schizophrenia
patients from Project 1 who were potential participants
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Schizophrenia Bulletin, Vol. 28, No. 4, 2002
K.L. Subotnik et al.
Andreasen, N.C.; Endicott, J.; Spitzer, R.L.; and Winokur,
G. The family history method using diagnostic criteria.
Archives of General Psychiatry, 34:1229-1235, 1977.
(13.3 years ± 2.5 SD). Thus, we have little reason to suspect that the educational level of these 98 subjects reflects
a selection bias within our sample. It is also possible that
parents who hold less critical attitudes toward their ill offspring or who exhibit fewer communication abnormalities
would be more likely to participate in two or more
research studies associated with the research clinic providing treatment for their offspring with schizophrenia. With
regard to EE status, our sample of participants in both
Projects 1 and 3 was not different than all participants in
Project 1 (53% in the current sample classified as high
CFI-EE versus 48% of all Project 1 participants). The present sample also did not appear to be biased in its distribution of TAT-CD scores in comparison to other studies.
Miklowitz et al. (1986) reported TAT-CD data on 205 relatives of schizophrenia patients drawn from three separate
sites in the United States that were very close to the mean
TAT-CD z score in the present study (mean = 0.13, SD =
0.41; Miklowitz et al. [1986] sample, mean = 0.15, SD =
0.36).
Another potential concern with this study is the use of
the SCID-II in a family history format. The SCID-II interview for the family history format is quite similar to that
for the direct interview format, and both use full
DSM-III-R criteria. Given that some personality disorder
symptoms may be more accurately rated based on the
reports of significant others rather than self-report, this
format may be especially valuable for personality disorders. Although we have shown good reliability for administration of the direct interview format (Fogelson et al.
1991), this novel use of the SCID-II has not been validated and needs further study.
In summary, we found that a family history of affective disorder is associated with lower rates of EE among
parents of schizophrenia patients. This suggests that prior
exposure to a severely depressed relative might promote
the development of more tolerant (i.e., lower EE) attitudes
toward one's own child as he or she struggles with a recent
onset of schizophrenia. In contrast, our CD results suggest
that high parental CD scores may be a vulnerability indicator for level of genetic loading for schizophrenia.
Although this genetic loading may not always express
itself in a frank psychotic disorder, it may result in cognitive deficits, one of which is tapped by the CD measure.
This type of family study, of course, cannot separate social
learning from genetic influences on CD, so further
research is needed to clarify the origins of CD.
Asarnow, R.F.; Granholm, E.; and Sherman, T. Span of
apprehension in schizophrenia. In: Steinhauer, S.R.;
Gruzelier, J.H.; and Zubin, J., eds. Handbook of
Schizophrenia. Vol. 5. Neuropsychology, Psychophysiology,
and Information Processing. Amsterdam, The Netherlands:
Elsevier, 1991. pp. 335-370.
Braff, D.L. Information processing and attention dysfunc-
tions in schizophrenia. Schizophrenia
Brown, G.W.; Birley, J.L.T.; and Wing, J.K. Influence of
family life on the course of schizophrenic disorders: A
replication. British Journal of Psychiatry, 121:241-258,
1972.
Brown, G.W., and Rutter, M. The measurement of family
activities and relationships: A methodological study.
Human Relations, 19:241-263, 1966.
Butzlaff, R.L., and Hooley, J.M. Expressed emotion and
psychiatric relapse: A meta-analysis. Archives of General
Psychiatry, 55:547-552, 1998.
DeLisi, L.E., and Crow, T.J. Evidence for a sex chromosome locus for schizophrenia. Schizophrenia Bulletin,
15(3):431-440, 1989.
Docherty, N.M., and Gordinier, S.W. Immediate memory,
attention, and communication disturbances in schizophrenia patients and their relatives. Psychological Medicine,
29:189-197, 1999.
Docherty, N.M.; Gordinier, S.W.; Hall, M.J.; and Cutting,
L.P. Communication disturbances in relatives beyond the
age of risk for schizophrenia and their associations with
symptoms in patients. Schizophrenia
Bulletin,
25(4):851-862, 1999a.
Docherty, N.M.; Rhinewine, J.P.; Labhart, R.P.; and
Gordinier, S.W. Communication disturbances and family
psychiatric history in parents of schizophrenia patients.
Journal of Nervous and Mental Disease, 186:761-768,
1999ft.
Fogelson, D.L.; Nuechterlein, K.H.; Asarnow, R.F.;
Payne, D.L.; and Subotnik, K.L. Validity of the family
history method for diagnosing schizophrenia, schizophrenia-related psychoses, and schizophrenia spectrum personality disorders in first-degree relatives of schizophrenic
probands. Schizophrenia Research, in press.
References
American Psychiatric Association.
Bulletin,
19(4):233-259, 1993.
Fogelson, D.L.; Nuechterlein, K.H.; Asarnow, R.F.;
Subotnik, K.L.; and Talovic, S.A. Interrater reliability of
the Structured Clinical Interview for DSM-III-R, Axis II:
Schizophrenia spectrum and affective spectrum disorders.
Psychiatry Research, 39:55-63, 1991.
DSM-III-R:
Diagnostic and Statistical Manual of Mental Disorders.
3rd ed., revised. Washington, DC: APA, 1994.
726
Communication Deviance and Expressed Emotion
Schizophrenia Bulletin, Vol. 28, No. 4, 2002
Gershon, E.S. "Relative Psychiatric History (RPH)
Symptom Checklist Interview." 1985. Available from Dr.
Elliot Gershon, Bldg 10, Room 3N218, National Institute
of Mental Health, Bethesda, MD 20892.
assessing expressed emotion in relatives of psychiatric
patients. Psychiatry Research, 17:203-212, 1986.
Miklowitz, D.J.; Goldstein, M.J.; Doane, J.A.;
Nuechterlein, K.H.; Strachan, A.M.; Snyder, K.S.; and
Magana-Amato, A. Is expressed emotion an index of a
transactional process? I. Parents' affective style. Family
Process, 28:153-167, 1989.
Goldstein, J.M. Gender and the familial transmission of
schizophrenia. In: Seeman, M.V., ed. Gender and
Psychopathology. Washington, DC: American Psychiatric
Press, 1995. pp. 201-226.
Miklowitz, D.J., and Stackman, D. Communication
deviance in the families of schizophrenic and other psychiatric patients: Current state of the construct. In: Walker,
E.F.; Dworkin, R.H.; and Cornblatt, B.A., eds. Progress in
Experimental Psychopathology Research. Vol. 15. New
York, NY: Springer, 1992. pp. 1^6.
Goldstein, M.J. The UCLA High-Risk Project.
Schizophrenia Bulletin, 13(3):505-514, 1987.
Goldstein, M.J.; Talovic, S.A.; Nuechterlein, K.H.;
Fogelson, D.L.; Subotnik, K.L.; and Asamow, R.F. Family
interaction versus individual psychopathology: Do they
indicate the same processes in the families of schizophrenics? British Journal of Psychiatry, 161(Suppl
18):97-102, 1992.
Miklowitz, D.J.; Strachan, A.M.; Goldstein, M.J.; Doane,
J.A.; and Snyder, K.S. Expressed emotion and communication deviance in the families of schizophrenics. Journal
of Abnormal Psychology, 95:60-66, 1986.
Gottesman, I.I. Schizophrenia Genesis. New York, NY:
Freeman, 1991.
Miklowitz, D.J.; Velligan, D.I.; Goldstein, M.J.;
Nuechterlein, K.H.; Gitlin, M.J.; Ranlett, G.; and Doane,
J. Communication deviance in families of schizophrenic
and manic patients. Journal of Abnormal Psychology,
100:163-173, 1991.
Hollingshead, A.B. 'Two-Factor Index of Social Position."
1957. Available from Dr. August B. Hollingshead,
Department of Sociology, Yale University, P.O. Box 208265,
New Haven, CT, 06520-8265.
Nuechterlein, K.H., and Dawson, M.E. Information processing and attentional functioning in the developmental
course of schizophrenic disorders. Schizophrenia Bulletin,
10(2): 160-203, 1984.
Hooley, J.M., and Gotlib, I.H. A diathesis-stress conceptualization of expressed emotion and clinical outcome.
Applied and Preventive Psychology, 9:135-151, 2000.
Hooley, J.M., and Hiller, J.B. Family relationships and
major mental disorder: Risk factors and preventive strategies. In: Sarason, B.R., and Duck, S., eds. Personal
Relationships: Implications for Clinical and Community
Psychology. New York, NY: Wiley, 2001. pp. 135-151.
Nuechterlein, K.H.; Dawson, M.E.; Gitlin, M.; Ventura,
J.; Goldstein, M.J.; Snyder, K.S.; Yee, CM.; and Mintz, J.
Developmental processes in schizophrenic disorders:
Longitudinal studies of vulnerability and stress.
Schizophrenia Bulletin, 18(3):387^25, 1992.
Jackson, H.J.; Smith, N.; and McGorry, P. Relationship
between expressed emotion and family burden in psychotic disorders: An exploratory study. Acta Psychiatrica
Scandinavica, 82:243-249, 1990.
Nuechterlein, K.H.; Goldstein, M.J.; Ventura, J.;
Dawson, M.E.; and Doane, J.A. Patient-environment
relationships in schizophrenia: Information processing,
communication deviance, autonomic arousal, and stressful life events. British Journal of Psychiatry, 155(Suppl
5):84-89, 1989.
Jones, J. Patterns of transactional style deviance in the
TAT's of parents of schizophrenics. Family Process,
16:327-337, 1977.
Robins, L.N.; Helzer, J.E.; Croughan, J.; and Ratcliff,
K.S. National Institute of Mental Health Diagnostic
Interview Schedule. Archives of General Psychiatry,
38:381-389, 1981.
Rosenfarb, I.S.; Goldstein, M.J.; Mintz, J.; and
Nuechterlein, K.H. Expressed emotion and subclinical
psychopathology observable within the transactions
between schizophrenia patients and their family members.
Journal of Abnormal Psychology, 104:259-267, 1995.
Kendler, K.S. Schizophrenia genetics. In: Sadock, B.J.,
and Sadock, V.A., eds. Comprehensive Textbook of
Psychiatry. Vol. 1. Philadelphia, PA: Lippincott, 2000. pp.
1147-1159.
Liang, K.H., and Zeger, S.L. Longitudinal data analysis
using generalized linear models. Biometrika, 13:13-22,
1986.
Liem, J.H. Effects of verbal communication of parents
and children: A comparison of normal and schizophrenic
families. Journal of Consulting and Clinical Psychology,
42:438-450, 1974.
Rosenfarb, I.S.; Nuechterlein, K.H.; Goldstein, M.J.; and
Subotnik, K.L. Neurocognitive vulnerability, interpersonal
criticism, and the emergence of unusual thinking by
patients with schizophrenia during family transactions.
Archives of General Psychiatry, 57:1174-1179, 2000.
Magana, A.B.; Goldstein, M.J.; Karno, M.; Miklowitz,
D.J.; Jenkins, J.; and Falloon, I.R.H. A brief method for
727
Schizophrenia Bulletin, Vol. 28, No. 4, 2002
K.L. Subotnik et al.
Shenton, M.E.; Solovay, M.R.; Holzman, P.S.; Coleman,
M.; and Gale, H.J. Thought disorder in the relatives of
psychotic patients. Archives of General Psychiatry,
46:897-901, 1989.
Spitzer, R.L.; Endicott, J.; and Robins, E. Research
Diagnostic Criteria: Rationale and reliability. Archives of
General Psychiatry, 35:773-782, 1978.
Spitzer, R.L.; Williams, J.B.W.; and Gibbon, M.
Structured Clinical Interview for DSM-III-R Personality
Disorders (SCID-II).
New York, NY: Biometrics
Research Department, 1987.
Wing, J.K.; Cooper, J.; and Sartorius, N. The
Measurement and Classification of Psychiatric Symptoms:
An Instruction Manual for the PSE and CATEGO
Programs. London, U.K.: Cambridge University Press,
1974.
Woo, S.M.; Goldstein, M.J.; and Nuechterlein, K.H.
Relatives' expressed emotion and non-verbal signs of subclinical psychopathology in schizophrenic patients.
British Journal of Psychiatry, 170:58-61, 1997.
Wynne, L.C., and Singer, M.T. Thought disorder and family relations of schizophrenics: I. A research strategy.
Archives of General Psychiatry, 9:191-198, 1963a.
Strachan, A.M.; Feingold, D.; Goldstein, M.J.; Miklowitz,
D.J.; and Nuechterlein, K.H. Is expressed emotion an
index of a transactional process? II. Patient's coping style.
Family Process, 28:169-181, 1989.
Wynne, L.C., and Singer, M.T. Thought disorder and family relations of schizophrenics: II. A classification of
forms of thinking. Archives of General Psychiatry,
9:199-206,19636.
Subotnik, K.L.; Nuechterlein, K.H.; Asarnow, R.F.;
Fogelson, D.L.; Goldstein, M.J.; and Talovic, S.A.
Depressive symptoms in the early course of schizophrenia: Relationship to familial psychiatric illness. American
Journal of Psychiatry, 154:1551-1556, 1997.
Wynne, L.C.; Singer, M.T; Bartko, J.J.; and Toohey, M.
Schizophrenics and their families: Recent research on
parental communication. In: Tanner, J.M., ed.
Developments in Psychiatric Research. London, U.K.:
Hodder and Stoughton, 1977. pp. 254-286.
Subotnik, K.L.; Nuechterlein, K.H.; Asarnow, R.F.;
Goldstein, M.J.; Fogelson, D.L.; and Torquato, R.D.
"Communication Deviance Is Associated With Putative
Genetic Vulnerability Indicators in Relatives of
Schizophrenia Patients." Paper presented at the biennial
meeting of the International Congress on Schizophrenia
Research, Santa Fe, NM, April 1999. [Schizophrenia
Research, 36 (special issue), 185.]
Acknowledgments
We thank Professor K.Y. Liang, School of Public Health,
Johns Hopkins University, Baltimore, MD, for giving us
the SAS macro code for the Generalized Estimating Equation analyses and for providing consultation on its use.
Responsibility for the analyses rests with us.
We would also like to thank the following individuals
for their assistance in collecting and/or coding the data
reported here: Jeri Doane, Ph.D.; Portia Loughman, B.A.;
Martha Magana, B.A.; Sandra Malik, B.A.; Margaret Rea,
Ph.D.; Karen Snyder, M.A.; Dawn Velligan, Ph.D.; and
Sybil Zaiden, B.A. We also acknowledge the statistical
services of Sun Hwang, M.S., M.P.H., of the University of
California, Los Angeles Clinical Research Center for
Schizophrenia (principal investigator: Robert P. Liberman,
M.D.).
This research was supported in part by National Institute of Mental Health grants MH37705, MH49716,
MH45112, MH30911, and MH08744 and by a grant from
the John D. and Catherine T. MacArthur Foundation.
Vaughn, C.E., and Leff, J.P. The influence of family and
social factors on the course of psychiatric illness: A comparison of schizophrenic and depressed neurotic patients.
British Journal of Psychiatry, 129:125-137, 1976.
Wagener, D.K.; Hogarty, G.E.; Goldstein, M.J.; Asarnow,
R.F.; and Brown, A. Information processing and communication deviance in schizophrenic patients and their
mothers. Psychiatry Research, 18:365-377, 1986.
Wahlberg, K.E.; Wynne, L.C.; Keskitalo, P.; Koistinen, P.;
Tarvainen, R.; Hakko, H.; Lahti, I.; Laksy, K.; Moring, J.;
Naarala, M.; Sorri, A.; Seitamaa, M.; and Tienari, P.
"Communication Deviance of the Adoptive Parents and
Poor Cognitive Functioning of the Adoptees." Paper presented at the Sixth Biennial Meeting of the International
Congress on Schizophrenia Research, Colorado Springs,
CO, April 1997a.
The Authors
Wahlberg, K.E.; Wynne, L.C.; Oja, H.; Keskitalo, P.;
Pykalainen, L.; Lahti, I.; Moring, J.; Naarala, M.; Sorri,
A.; Seitamaa, M.; Laksy, K.; Kolassa, J.; and Tienari, P.
Gene-environment interaction in vulnerability to schizophrenia: Findings from the Finnish adoptive family study
of schizophrenia. American Journal of Psychiatry,
154:355-362, \997b.
Kenneth L. Subotnik, Ph.D., is Associate Research Psychologist and Adjunct Associate Professor, Department of
Psychiatry and Biobehavioral Sciences; Michael J. Goldstein, Ph.D., (deceased) was Professor in the Departments
of Psychology and of Psychiatry and Biobehavioral Sciences; and Keith H. Nuechterlein is Professor in the
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Communication Deviance and Expressed Emotion
Schizophrenia Bulletin, Vol. 28, No. 4, 2002
Departments of Psychiatry and Biobehavioral Sciences
and of Psychology, University of California, Los Angeles.
Stephanie M. Woo is Assistant Professor of Psychology,
Pepperdine University, and Assistant Clinical Professor of
Psychiatry and Biobehavioral Sciences, University of California, Los Angeles. Jim Mintz is Professor in the Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles.
729