EUROPEAN JOURNAL OF INFLAMMATION Vol.8, no. 3.

211-219(2010)

COGNITIVE IMPAIRMENT AND PERCEIVED STRESS IN SCHIZOPHRENIC

INPATIENTS WITH POST-TRAUMATIC STRESS DISORDER

R. POLLICE, V. BIANCHINI, CM. CONTI', M. MAZZA, R. RONCONE

atid M. CASACCHIA

Psychiatric Unit, Department of Health Sciences, University ofL 'Aquila and San Salvatore
Ho,spital, L 'Aquila; 'Department of Psychology, University of Chieti, Chieti, Italy

Received February 4, 2010-Accepted September 22, 2010 •'''

The rate of lifetime traumas in the general population is high and a great deal of evidence suggests
that persons with severe mental illness (SMI) show an even higher degree of vulnerability to trauma
throughout their lives. Recent studies report between 13 and 29% of eomorbid Post-Traumatic Stress
Disorder (PTSD) in schizophrenic patients. Other studies showed that SMI patients with PTSD were in
poorer health, had lower self-esteem, and had lower subjective quality of life and more cognitive deficits in
comparison with those without PTSD. The aim of this work is to study a sample of chronic schizophrenic
inpatients admitted after the L'Aquila earthquake, to assess if eomorbid PTSD is associated with a higher
rate of neurocognitive deficit and poorer quality of life in comparison with schizophrenic inpatients
without PTSD. The sample of this study, recruited after the L'Aquila earthquake (between April 2009
and December 2009), consisted of 54 schizophrenic earthquake survivors admitted consecutively to the
Psychiatric Inpatients Unit of L'Aquila San Salvatore Hospital. Each patient was assessed with the Positive
and Negative Syndrome Scale (PANSS) and the General Health Questionnaire - 12 items (GHQ-12). The
Impact of Event Scale-Revised (lES-R) was used to grade post-traumatic symptoms. PTSD diagnosis
was made with the Structural Clinical Interview for DSM-IV (SCID-I). The cognitive assessment battery
included WAIS-III Digit Span and Trail Making Test to assess working memory and executive functions,
respectively. The severity of illness was measured with the Clinical Global Impression Scale (CGI). All the
patients were on antipsychotic drugs at a mean daily chlorpromazine-equivalent dose of 236.38 mg (SD
183.5). 17% of the 54 schizophrenic inpatients (n 9) met the DSM-IV criteria for PTSD. PTSD subjeets
had significantly higher scores on the PANSS Positive Symptom subscale (P< 0.015) and higher GHQ-12
mean score ( 30.50 i'.v 16.93). In the presence of post-traumatie symptoms a significant difference between
the two groups (with and without PTSD) was found in hyper-arousal subscale scores, with a significant
impairment of working memory in the PTSD sample. PTSD symptom measures positively correlated with
the PANSS total and Positive score and GHQ-12 score > 20 ("high stress level"). PTSD in schizophrenic
patients is associated w ith a more severe cognitive deficit, higher levels of perceived stress and more positive
symptoms. The investigation of PTSD in patients with schizophrenia might have important implications
for their clinical management and for future research.

At 3.32 a.m. on April 6, 2009, an earthquake registering 6.3 on the Richter scale struck L'Aquila,

¡ Key words: earthquake, PTSD, schizophrenia, stress, cognitive impairment

Mailing address:
Rocco Pollicc,
Department of Health Science.
University of L'Aquila,
Via Vetoio. Loc. Coppito. 67100 L'Aquila
Tel: ++39 0862368314 Fax: ++39 0862312104
e-mail: rocco.pollice(a)cc.univaq.it
0393-974X(2010)
Copyright ii'i by BIOLIFE, s.a.s.
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212 R. POLLICEETAL.
a town in central Italy, causing about 300 deaths and
2,500 severe injuries; 65% of building and homes
were damaged or destroyed. After the earthquake
approximately 25,000 victims were forced to
relocate on the east coast of Abruzzo and about
35,000 victims were relocated elsewhere in various
camp tents. Earthquakes and other disasters are
known to precipitate psychiatric symptoms, and the
increased risk of post-disaster psychiatric morbidity
includes higher levels of direct exposure or property
damage, the presence of a prior psychiatric disorder,
coping by avoidance, and lower social support (1-4),
Trauma and post-traumatic stress disorder (PTSD)
have high prevalence among individuals with SMI,
such as schizophrenia. Between 69.5 and 98% of this
population experienced a traumatic event in their life
(5-7) compared to 39-56% in the general population
(8-9). Rates of current PTSD in individuals with a
severe mental illness range from 29 to 48% (10-13).
These rates are much higher than the prevalence
of lifetime PTSD in the general population which
ranges from 7.8 to 9.2% and the point prevalence of
2% (7-8).
Several studies have shown that schizophrenic
subjects often report PTSD symptoms related to
the onset of their psychosis (14). The avoidance
of trauma-related stimuli often extends to close
relationships, leading to reduced social contacts and
social isolation (15), Some researchers believe that
social isolation may increase the vulnerability to
psychotic symptoms due to the lack of opportunities
for shared reality testing and the absence of
meaningful social stimulation such as work. Thus,
PTSD-induced severe avoidance and social isolation
in persons with schizophrenia are expected to worsen
their symptoms and related deficits in other areas of
functioning (16), Evidence shows that both specific
Stressors (e.g. life events or an earthquake) and
exposure to chronic stress may lead to a worsening
of SMIs, resulting in symptom relapse and re-
admission to hospital. Persons with schizophrenia
who re-experience traumatic events in the form of
intrusive memories, nightmares, or flashbacks may
be at increased risk of relapses due to the stressful
effects of such phenomena. Over-arousal, the third
symptom cluster of PTSD, is also linked to a worse
prognosis of SMI. Several studies have shown
that increased physiological arousal, particularly
chronic autonomie arousal, is associated with a
poor prognosis in persons with SMI. In a sample of
SMI patients, mainly suffering from schizophrenia
or schizoaffective disorders, the subjects with
comorbid PTSD were in poorer health, had lower
self-esteem, and had lower subjective quality of
life compared to those without PTSD (17). Another
study reported that, among elderly males diagnosed
with schizophrenia, comorbid PTSD was associated
with decreased health-related quality of life and
increased utilization of medical services (18).
Only a few studies exist on the impact of comorbid
PTSD on cognitive function in schizophrenia.
Several neuropsychological investigations document
the presence of a deficit in many cognitive domains
after exposure to Stressors such as an earthquake, but
the type and severity of the cognitive impairment
(executive function, verbal memory, working
memory, etc) differ between studies, and the causes
of the problem remain poorly understood. The
cognitive deficit seems to be particularly severe
among individuals with severe mental illness
like schizophrenia (19). The severity of cognitive
symptoms in these subjects is strongly correlated
with an impairment of social and occupational
functioning and lower quality of life (QOL) (20-22).
Although trauma and PTSD are common among
patients suffering from a severe mental illness, their
impact is frequently overlooked by clinicians.
The aim of this work is to study a sample of
chronic schizophrenic inpatients admitted after
the L'Aquila earthquake, to assess whether PTSD
cornorbidity is associated with a higher rate of
neurocognitive deficit and poorer quality of life in
comparison with schizophrenic inpatients without
PTSD.
MATERIALS AND METHODS
Sample
L'Aquila is located in the eentre of Italy, and before
the oeeurrenee of a devastating earthquake registered
as 6,3 magnitude on Riehter Seale had a population of
about 70,000 people. In the region struck by the quake,
308 people were killed and 2,500 severely injured; 65%
of buildings and houses were damaged or destroyed. This
study was eondueted after the disaster (between April 2009
and December 2009), on a sample of 54 sehizophrenie
patients eonseeutively admitted to the Psychiatry Ward
 European Journal of Inflammation
of L'Aquila San Salvatore Hospital. The subjects with a
diagnosis of schizophrenia were referred to the study by
their Case Manager. The diagnosis was further confirmed
by a research psychiatrist with the DSM-IV Structural
Clinical Interview (SCID) (23). The Case Managers were
informed about the study protocol and were requested
to select the patients who met the inclusion criteria
and to obtain their permission to disclose their names
to the investigators. Inclusion criteria were: minimum
age 18 years; organized speech; good understanding
of the interview questions. Exclusion criteria were
severe medical problems preventing participation, fiorid
psychotic condition or too chaotic speech preventing
sufficient communication. All the recruited subjects gave
written informed consent to participate in the study. The
study protocol was approved by the Ethical Committee.
All patients were taking traditional and/or atypical
antipsychotic drugs. Any attempt to reduce or discontinue
drug administration induced a clinical worsening. Despite
the use of medication, after the earthquake the subjects
had shown a general clinical worsening rated with CGI
score between 4 (moderately ill) and 5 (severely ill).
Antipsychotic treatment was started in add-on open-
label regime and drugs were progressively increased as
clinically tolerated to the therapeutic dosage (300-1,000
mg/die Chlorpromazine equivalent doses - Haloperidol
6-20 mg; Flufenazine 6-20 mg; Perfenazine 12-64 mg;
Risperidone 2-4 mg; Olanzapine 10-20 mg; Quetiapine
300-750 mg; Arpiprazole 10-30 mg; Paliperidone 3-15
mg). This protocol was maintained for the entire duration
ofofthe study (24-25).
In case of need, patients were also given lorazepam, 2.5
mg orally p.m., for sleep or agitafion and/or orfenadrine
on demand for acute extrapyramidal symptoms. No other
psychotropic drugs were permitted. The clinical evaluation
was performed at baseline and repeated on discharge from
the inpatient ward. 40.9% of subjects reported a moderate
to marked improvement on the CGI Clinical improvement
scale, 54.6% of them improved mildly, whereas 4.5%
worsened or remained unchanged.
Instruments
Clinical Assessment
Clinical symptoms were assessed with the Positive
and Negative Syndrome Scale (PANSS), including
Positive Symptom, Negative Symptom, and General
Psychopathology sub-scales (26). The General Health
Questionnaire (GHQ-12) consists of 12 items, each
assessing the severity of mental problems over the
previous few weeks using a 4-point scale (from 0 to 3).
This tool can be used to check the likelihood of a clinical
illness on the basis of cut-off scores and to determine the
severity of symptoms by total scores. Sensitivity and
213
specificity in the prediction of psychiatric morbidity were
69.6 % and 94.8%, respectively, in this community study.
The method was used to generate a total score ranging
from 0 to 36: a score < 15 indicates a nonnal stress level,
a score between 15 and 20 stands for a moderate level of
stress, while a seore > 20 indicates a severe condition of
stress (27).
Assessment of Post-Traumatic Stress Di.sorder (PTSD)
The Impact of Events Scale (IES) (28) is a well known
self-report measure of symptoms associated with PTSD;
it was used here to assess the psychological impact of
the earthquake. The IES consists of 15 items that the
participants employed to rate how frequently they had
experienced a variety of reactions to the Earthquake
during the previous seven days; results were expressed on
a four-point scale ranging from "not at all" to "often". The
IES includes two sub-scales: Intrusion and Avoidance,
to assess separable but moderately correlated constructs
(r=0.63). IES Intrusion items are related to re-expericncing
a range of eognitive reactions to the earthquake. IES
Avoidance items refer to avoiding or minimizing thoughts
or emotions associated with the event. Alpha coefficients
for both sub-scales were good across assessments for
schizophrenia (range=0.84-0.86) (28). The subjects with
PTSD diagnosis were referred to the study by a research
psychiatrist after administration of the Structural Clinical
Interview for DSM-IV (SCID) (23).
Neuropsychological test
All the participants to the study undertook the WAIS-
III Digit Span test to check their working memory (29).
Severity of Illness
The Clinical Global Impression Scale (CGI severity
and improvement) was used to assess the severity of
mental illness an global improvement. Item 1 is rated
on a seven-point scale (l=nomial to 7=extremely ill);
item 2 on a seven-point scale (l=very much improved to
7=very much worse). The "Severity of Illness" item was
used to rate the severity of the patient's condition, taking
into account the elinician's past experience with subjects
having the same diagnosis. The Global improvement item
is used to rate how much the patient's illness has improved
or worsened over time with respect to baseline state.
Statistical analysis
A statistical analysis was performed using SPSS
(version 14.0). In all cases, a P value lower than 0.05
(2-tailed) was used to express statistical significance.
The demographic and clinical characteristics of the study
sample were submitted to a descriptive statistical analysis.
Group comparisons were performed using independent
214 R. POLLICE ETAL,

/-tests for continuous variables and chi-square tests for
categorial variables. Pearson's correlation analysis was
used to explore the relationships among continuous
variables.
The global cognitive performance was compared
between PTSD and non-PTSD groups using the one-way
multivariate analysis of variance (MANOVA). Only the
significant MANOVA results were further processed
with univariate analysis of variance (ANOVAs) to check
individual cognitive variables.
RESULTS
Sample re.sults
The socio demographic features of the total
sample (N=54) are shown in Table I.
All schizophrenic subjects were aged over 18
years. Mean age was 44.6 (SD ±14.1) years: 30.8%
of the sample were women and 69.2% men; mean
education was 5.6 years (s,d,= ±3,2), 22,8% were
employed versus 87.2% without a joh. 57.4% were
single, 24.4% and 18.2% were, respectively, married
and separated or divorced.
Mean time of hospitalization was 13.31 (s,d.±
9,67) days: 10,19 (s.d, ±6,9) days for men and
15.79 (s.d. ±10.8) for women. Mean duration of
Schizophrenia was 17,3 years (±7.4),
All the patients were in L'Aquila at the time of
the disaster. None of the subjects had close relatives
killed in the earthquake; 11,4% of the sample were
injured. Approximately 83% of the subjects reported
that their houses had been destroyed or mildly
damaged versus 17% of houses left undamaged,
56,4 % of the inpatients had a moderate level of
stress (GHQ-12 >15), while 21,4 % suffered a
high level of stress (GH0-12> 20) Fig, 1, When
assessed with IES-R, 23,3% of the sample showed
post-traumatic symptoms : 15,4% were positive
for avoidance subscale, 36.1% for hypcr-arou,sal
scale and 21.3% for re-experience. A significant
correlation was found between high GHQ-12 (>
20) and gender hyper-arousal (p< .045). 32.4% of
the sample had poorer neurocognitive performance

Table I. Socio-demographic features: total sample.

Total sample (N=54)

Age Mean (s.d.) 44.6 (±14.1) years

Male (%) 69.2%
Female (%) 30.8%
Education Mean (s.d.) 5.6 ( ± 3.2) years
Employed (%) 22.8%
Unemployed (%) 87.2%
Single (%) 57.4 %
Married (%) 24.4%
Separated/divorced (%) 18.2%
Presence at time of earthquake (%) 100%
Gain (%) 0%
Injured (%) 11.4%
Houses destroyed or damaged (%) 83%
Houses undamaged (%) 17%
Hospitalization 13.31 (±9.67) years
Schizophrenia duration 17.3 (±7.4) years

Together with socio-demographic characteristics, this table shows a summary of the level of exposure to the earthquake
and of the environmental variables most frequently reported in the literature in association with psychopathological
consequences.
 European Journal of Inflammation
60-1
GHQ-12
Fig. \. All patients' GHQ-12 score percentage. General
Health Questionnaire is used to identify a "probable
clinical case " on the basis of perceived stress level. In our
sample, youths .seem to he worse than children or adults.
reexperjence
11
iperarousal
P D lES-R positive
sample
avoidance
y
Í y y
0 10 20 30 40
Fig. 2. lES-R positive sub-scale percentage. The
psychological impact of the earthquake was assessed
with the Impact of Events Scale (IES), a widely used self-
report measure of symptoms associated with PTSD. IES
cotnprises two subscales. Intrusion and Avoidance. IES
Intrusion items involve re-experiencing various cognitive
reaction about the Earthquake. IES Avoidance Items
refer to avoiding or minimizing thoughts or emotions
associated with the event.
scores on working memory tests (Digital Span B).
Nine of the 54 sehizophrenia patients (17%) met
DSM-IV criteria for PTSD assessed with SCID-I.
PTSD vs non-PTSD comparison
When the subjects meeting the criteria for PTSD
(group "A") were compared with the subjects who
did not ("B"), no difference was found for items
such as age, educational level, marital status,
employment status, duration of schizophrenia and
of hospitalization; some difference was reported
215
for gender ( A: 66.7% female and 33.3% male; B:
83.3% male vs 16.7% female) Table II Group A had
significantly higher scores on the Positive Symptom
subscale, (P < .015). No significant difference was
observed between Group A and Group B on the
PANSS Total, Negative Symptom and General
Psychopathology subscale. GHQ-12 mean score is
higher in Group A than in Group B (30.50 vs 16.93),
but the difference is not significant ( p < .9). The
comparison of post-traumatic symptoms in tbe two
groups showed a significant difterence in hyper-
arousal subscale (p < .04). Furthermore, the PTSD
group had significantly worse working memory
performance in Digital Span B ( p< .05) than the
non-PTSD group (see Table III). PTSD symptom
measures positively correlated with PANSS total
score and Positive subscale (P < .002). In contrast,
no relationships was found between PTSD symptom
measures and the GHQ-12 score < 20 (P< .80), apart
from GHQ-12 score >20 "high stress level" (p<
.002). The comparison of cognitive performance
between PTSD Groups A and B showed that working
memory global performance was worse in Group A
than in the non-PTSD group (P=0.02).
DISCUSSION
Trauma and PTSD have been related to a variety
of negative outcomes in patients with schizophrenia.
Patients with PTSD tend to have more severe
psychotic symptoms (14), increased suicidality
(30), and greater need of psychiatric services (8).
Adding to the existing literature, the present study
specifically examined PTSD and schizophrenia
in relation to cognition and quality of life. Our
study suggests that for patients with schizophrenia
and a history of trautna exposure, those who have
developed PTSD suffer greater cognitive impairment
particularly in the domains of attention, working
memory and executive function compared with non-
PTSD subjects. These findings arc consistent with a
recent report based on a sample of elderly patients
with chronic schizophrenia (7).
Stress-related changes in specific brain areas
might underlie the worsening of cognitive function
in patients with schizophrenia and comorbid PTSD.
Altematively, among schizophrenic patients exposed
to trauma, those who develop PTSD might have
216 R. POLLICE ETAL.

Table II. Comparison of socio-demographic features between PTSD and non-PTSD groups.

Features Group A Group B

(N=9) (N= 39)
"PTSD diagnosis" " non-PTSD"
Age Mean (s.d.) 44.5 (15.46) years 44.3(10.2)
Male (%) 33.3% 83,3%
Female (%) 66.7% 16,7%
Education Mean (s.d.) 5.6 ( ± 3.2) years 5.2 ( ±4.2) years
Employed (%) 18.3% 23.3 %
Unemployed (%) 81.7% 76.7%
Single (%) 62.2 % 64.1%
Married (%) 19.8% 23.2%
Separated/divorced (%) 18% 12.7%
Present at time of 100% 100%
earthquake (%)
Gain (%) 0% 0%
Injured (%) 12.1% 8.9%
Houses destroyed or 84.1% 81.2%
damaged (%)
Houses undamaged (%) 17.1% 16.5%
Hospitalization 13.31 (±9.67) years 12.9 (±9.5) years
Schizophrenia duration 16.8 (±7.4) years 17.9 (±6.9)

lower premorbid cognitive function to begin with in
comparison with those who do not develop PTSD.
Retrospective case control studies suggest that low
intelligence level is a risk factor for developing PTSD.
It is speculated that individuals with low intelligence
are less effective in coping with trauma compared
to those with higher intelligence score. Quality
of hfe and level of ñmctioning hav proved to be
increasingly important parameters in the assessment
of treatment outcome in patients with schizophrenia
(30). In patients with severe mental illness, PTSD
may contribute to a decline in the quality of life (7-8,
24). In line with previous findings, this study shows
that among schizophrenic patients with a history of
trauma exposure, those who have developed PTSD
report a subjectively experienced poorer quality of
life when compared with subjects with no PTSD.
Other studies have suggested that patient-rated QoL
and observer-rated QoL in schizophrenic patients
appear to have different determinants. Patient-
rated QoL may be strongly influenced by anxiety
and depression symptoms, whereas the severity of
negative symptoms is an important deteraiinant for
observer-rated QoL (30). In our study, the PTSD
group appeared to have more anxiety and depression
symptoms, as measured by the PANSS General
Psychopathology sub-scale. However, no difference
was found in negative symptoms as measured by the
PANSS Negative Symptoms subscale. Therefore, it
is not surprising that the PTSD group subjectively
experienced a poorer quality of life compared with
the non-PTSD group, even though no difference
was found between the two groups in observer-rated
quality of life.
PTSD is typically under-diagnosed in patients
with severe mental illness (19). Presumably,
PTSD is even more likely to be overlooked in
patients with schizophrenia since a considerable
overlap exists between the diagnostic constructs of
schizophrenia and PTSD (9, 14, 29). As an example,
the negative symptoms of schizophrenia might
look like avoidance or numbing features in PTSD;
"flashback" experiences in PTSD might be easily
taken for hallucinatory symptoms of schizophrenia.
The Evaluation of PTSD in patients with
schizophrenia might have important implications in
 European Journal of Inflammation
217

Tal)le III. Clinical, psychometric and cognitive evaluations: comparison between the PTSD and the non-PTSD group.

Group A Group B Comparison

"PTSD diagnosis" " non-PTSD"

PANSS total 1 73,5 69,9 .456

PANSS negative 19,6 18,9 .6
PANSS positive | 26 14,6 <.O15
PANSS general 33.1 34,6 .66

GHQ-12 score 30,50 16,93 ,9

IES-R avoidance 9 (±2,8) 9,33 (±5,3) ,4

IES-R 26 (±12,1) 12,17 (±13,7) ,02
hyperarousal
IES-R reexperience 7,50 (±0,7) 8,75 (±5,7) ,1

Digital Span A 3 (±1,7) 4,17 (±1,1) .3

Digital Span B 2.67 (±1.1) 3,09 (±0,5) .05

The PTSD group apparently had more anxiety and depression symptoms as measured by the PANSS General
P.sychopathology sub-scale. However, there was no difference in negative .symptoms as measured by the PANSS Negative
Symptoms sub-scale. Therefore, it is not .surprising that the PTSD group experienced a poorer quality of life (as perceived
stre.ss levels) .subjectively compared with the non-PTSD group, even though no difference in obser\'er-rated quality of life
was reported between the two groups.

terms of clinics and research. For those patients who
are reluctant to reveal previous trauma history, PTSD
might be misdiagnosed as schizophrenia, or simply
missed as a comorbid condition in schizophrenic
patients. Unrecognized and untreated PTSD might
eventually lead to labeling some of the patients with
schizophrenia as "treatment resistant". In recent
years, NIMH has taken the initiative to support the
development of new drugs to improve cognition
in schizophrenia (28), Since PTSD is associated
with poor cognitive performance, as suggested by
our findings, it is important to consider PTSD as
a confounding factor in future clinical trials about
the cognitive function in schizophrenia patients.
Our study suffered from several limitations and its
cross-sectional design made it impossible to find any
causal relationships among PTSD, schizophrenia
and functional measures. Since most of the subjects
recruited in this study had low socio-economic status
and chronic mental illnesses, the findings might
not be generalized to schizophrenia patients with
relatively higher socioecon'omic status or those in an
earlier phase of illness. Furthermore, it was unclear
whether the subjects experienced some traumatic
events before or after the onset of schizophrenia.
Therefore, an important question remains open:
should we regard trauma as an element contributing
to the development of schizophrenia or rather as a
factor complicating the clinical manifestation of
schizophrenia? Longitudinal studies are needed to
further investigate the relationship between PTSD
and schizophrenia, as well as the impact of such
comorbid conditions on cognition and real life
functioning.
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