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Intrusive prospective imagery, posttraumatic intrusions and anxiety in schizophrenia
Psychiatry Research 230 (2015) 899–904
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Intrusive prospective imagery, posttraumatic intrusions and anxiety in schizophrenia Charlotte P. Malcolm a,n, Marco M. Picchioni b,c, Lyn Ellett a a
Department of Clinical Psychology, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK Institute of Psychiatry, King’s College, University of London, London SE5 8AF, UK c Academic Centre, St. Andrew’s, Cliftonville, Northampton NN1 5DG, UK b
art ic l e i nf o
a b s t r a c t
Article history: Received 29 March 2015 Received in revised form 30 September 2015 Accepted 17 November 2015 Available online 19 November 2015
Trauma exposure and intrusive thoughts are commonly reported in both schizophrenia and posttraumatic stress disorder (PTSD). Information processing accounts suggest that intrusions occur in the two conditions as a result of insufficient state and/or trait contextual processing in long-term memory. Most research has focused on intrusions about past events, while growing evidence suggests that intrusions about prospective imagined events warrants further investigation. Prospective intrusive imagery has yet to be examined in psychotic disorders but could provide crucial information regarding the aetiology and maintenance of psychotic symptoms. The current study examines the role of prospective intrusive imagery, posttraumatic intrusions and anxiety in schizophrenia. Fifty-seven participants (30 patients and 27 healthy controls) completed measures of trauma, PTSD, anxiety, general non-affective use of imagery, and intrusive prospective imagery. Patients reported significantly more intrusive prospective imagery relative to control participants but, importantly, not greater use of general non-affective imagery. Intrusive prospective imagery was associated with posttraumatic intrusions and anxiety in schizophrenia. The findings are consistent with information processing models of intrusions and psychosis, and provide novel insights for theoretical accounts, clinical formulation and therapeutic targets for psychotic symptoms in schizophrenia. & 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Psychosis PTSD Trauma Stress Hallucinations Cognition
1. Introduction A well-established link exists between trauma exposure and the development of schizophrenia (e.g. Bebbington et al., 2004; Bendall et al., 2010; van Os et al., 2010). Research finds varying rates of co-morbid PTSD in schizophrenia from around 13% to 53% (Mueser et al., 1998; Resnick et al., 2003; Howgego et al., 2005; Kilcommons and Morrison, 2005) with large differences in findings likely due to differing methodology (e.g. self-report versus clinical assessment; see Mueser et al., 2001) and the clinical context. However, the findings suggest higher rates of PTSD in schizophrenia than would be expected in the general populationaround 7.8–9.2% (Breslau et al., 1991; Kessler et al., 1995). Psychotic symptoms are also frequently and co-morbidly reported with PTSD (Anketell et al., 2010). However, the pathophysiological link between trauma and schizophrenia still remains unclear. To elucidate this link current research has explored common features and shared vulnerability factors for PTSD and schizophrenia. n
Corresponding author. E-mail address: [email protected] (C.P. Malcolm).
http://dx.doi.org/10.1016/j.psychres.2015.11.029 0165-1781/& 2015 Elsevier Ireland Ltd. All rights reserved.
Intrusive cognitions are a transdiagnostic feature of both PTSD and schizophrenia and may shed light on underlying cognitive mechanisms linking the two disorders. Intrusions are involuntary, unbidden cognitions, regarded as the “hallmark” of PTSD (Ehlers and Clark, 2000), but now considered to play a role in a range of other psychological disorders, including schizophrenia (Brewin et al., 2010; Morrison, 2001). Intrusions are believed to arise due to insufficient contextual integration during information processing and storage into long-term memory (Brewin, 2001; Brewin et al., 2010; Ehlers and Clark, 2000). Contextual integration, a function of the hippocampus, involves the processing and storage of autobiographical information with corresponding temporal and spatial information. Without adequate contextual processing, memory traces become disconnected from their temporal-spatial context; such that when the memory trace is triggered it intrudes into consciousness with a sense of “nowness” (Ehlers and Clark, 2000). During a traumatic event, information is processed rapidly via the amygdala with limited contextual integration, resulting in intrusions in the form of re-experiencing (e.g. “flashbacks”). For example, a year after an individual was involved in a terrifying car accident they may re-experience an intrusive image of the crash
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with a sense that it is happening in the present moment when they hear the screech of a car breaking. Cognitive models locate intrusions, and particularly the appraisal of intrusions, as central in the development and maintenance of psychotic phenomena (e.g. Morrison, 2001; Garety et al., 2001; Morrison et al., 2002; Read et al., 2005). Patients who experience positive psychotic symptoms are also more likely to report intrusions than other psychiatric and healthy control groups (Morrison and Baker, 2000; Morrison et al., 2002). Research has identified an attribution bias in individuals with psychosis whereby there is a tendency to attribute intrusions to external and malign sources (rather than internally generated memories) leading to emotional distress when intrusions are experienced (e.g. Bentall, 1990). The intrusion is then unwittingly maintained through maladaptive coping such as thought suppression or paranoid hypervigilence (Beck and Rector, 2003). Further, research (Steel et al., 2005; Fowler et al., 2006) has extended the cognitive models of memory processing (e.g. Brewin et al., 2010) to psychosis, identifying a “catastrophic interaction” between an underlying cognitive processing deficit and previous trauma in schizophrenia. Steel et al. (2005) cite evidence from experimental paradigms of context-dependent memory that baseline contextual processing is weaker in schizophrenia, conferring vulnerability to more frequent intrusions. Subsequent research has consistently found specific impairments in contextdependent memory and hippocampal function in schizophrenia, relative to non-context dependent memory, which remains intact (e.g. Weniger and Irle, 2008; Zierhut et al., 2010). Steel et al. (2005) further posit that past trauma results in emotional experiences that are insufficiently integrated in time and place, leading to a sense of current ongoing threat that influences the appraisal of intrusions. Intrusions from past long-term memory have received considerable theoretical attention (e.g. Ehlers and Clark, 2000; Brewin et al., 2010) but only provide a limited insight into the nature and consequences of intrusions. A large body of research over the past decade has provided consistent evidence that thinking about the future recruits the same cognitive processes and neural circuitry as remembering the past (see Szpunar et al., 2014 for a review), in part through the extraction and recombination of stored information to simulate a novel prospective event, leading to the concept of the “prospective brain” (Schacter et al., 2007). The concept of the prospective brain has led to an interesting line of research exploring how we can apply the vast body of knowledge of retrospective memory to understanding and enhancing cognition for future events (e.g. McLelland et al., 2014). Likewise, drawing on the concept of the prospective brain, Deeprose and Holmes (2010) have argued that intrusions about future events, specifically intrusive imagery, which exerts a stronger influence on emotions than verbal cognition (Beck, 1976), warrant further investigation. Historically it has been assumed that one must have already experienced an unpleasant event to experience intrusions for that event. Deeprose and Holmes (2010) have challenged that assumption, finding evidence that individuals report “flashforwards” or “pre-experiencing” of imagined future events, known as prospective intrusive imagery. Flashforwards exhibit the same phenomenological qualities as intrusive memories for past events: they are unbidden, involuntary and are accompanied by a sense of “nowness” (Holmes et al., 2007). Negative and distressing intrusions (e.g. a flashforward to the individual carrying out a suicidal act), maintain depression by perpetuating low mood (Deeprose and Holmes, 2010). Prospective intrusive imagery is associated with greater mood instability in bipolar disorder (Holmes et al., 2011) and greater state anxiety and depression in a range of affective disorders (Morina et al., 2011). There has been no work to date on prospective intrusive imagery in psychotic disorders but,
based on cognitive models of psychosis, it is expected that greater intrusive prospective imagery would be present in patients with schizophrenia. Anxiety is also common in schizophrenia (Braga et al., 2005) and exacerbates psychotic symptoms (Huppert and Smith, 2001). If present in schizophrenia, intrusive prospective imagery may similarly contribute to the positive symptoms and the elevated rates of anxiety in schizophrenia. The aims of this study were to investigate the presence of intrusive prospective imagery in schizophrenia relative to healthy controls, and identify the relationship between intrusive prospective imagery, retrospective intrusions and anxiety in schizophrenia. It was hypothesised that (1) individuals with schizophrenia will experience greater intrusive prospective imagery than controls, and (2) within the clinical group, prospective intrusive imagery will be positively associated with anxiety and retrospective intrusions in the form of posttraumatic re-experiencing.
2. Methods The research was approved by the London Stanmore (ref.: 12/ LO/0813) and Royal Holloway, University of London Psychology Department Ethics Committees (ref.: 2012/056). Patients completed measures in face-to-face interviews with the same researcher. Control participants completed measures in face-to-face interview format or as self-report measures depending on preference. 2.1. Participants Fifty-seven participants comprising patients (N ¼30; 22 male) and healthy controls (N ¼27; 16 male) were recruited. Sample size was determined by an a priori power calculation in line with Cohen's (1988) conventions to detect a large effect size (R2 40.05) in a correlational analysis, with alpha set at 0.05 and beta set at 0.2 (thus power is set at 0.8). The patients were formally diagnosed by a consultant psychiatrist with an ICD-10 (F20-21 and F25-25.9) schizophrenia spectrum disorder and recruited from 12 inpatient mental health wards in the south of England. All of the patients reported current positive symptoms, with most (N ¼26) reporting hallucinations. The control group was recruited through advertisements online and in public buildings. Participants were included if they were aged between 18 and 65 and provided written informed consent after a full description of the study. Patients were included if they had a diagnosis of a schizophrenia spectrum disorder. Exclusion criteria were history of significant head injury (loss of consciousness 45 min), neurological disorder or organic psychosis, current substance misuse, diagnosis of a personality disorder, poor comprehension of English, or an IQ of less than 70. Control participants were excluded if they reported a mental health diagnosis or symptoms of psychosis on the SCID IV psychosis screen (First et al., 1996). Control participants were excluded if they reported a trauma in addition to posttraumatic stress symptoms that constituted criteria for diagnosable PTSD as measured by the Posttraumatic Stress Diagnostic Scale (PDS; Foa, 1997). 2.2. Measures Hospital Anxiety and Depression Scale (HADS; Zigmond and Snaith, 1983): is a 14-item measure used to detect current symptoms of depression and anxiety and is a valid predictor of diagnosis and severity of depression and anxiety disorders (Bjelland et al., 2002). The HADS is composed of two subscales: HADS-A (7 items to detect anxiety) and HADS-D (7 items to detect depression). The HADS has good reliability for detecting anxiety and
C.P. Malcolm et al. / Psychiatry Research 230 (2015) 899–904
depression in schizophrenia (Allan and Martin, 2009). Positive and Negative Symptom Scale (PANSS; Kay, 1991) is the most widely used measure of symptoms of schizophrenia from the previous 72 h and is administered in interview format. The PANSS represents three separate subscales: positive, negative and general symptoms and has well-established reliability and validity (Kay et al., 2000). Posttraumatic stress diagnostic scale (PDS; Foa, 1997) is a selfreport measure of lifetime trauma type and posttraumatic symptom severity. The items reflect the DSM-IV diagnostic criteria for PTSD, including a subscale for re-experiencing, avoidance and arousal symptoms. The PDS is a valid and reliable measure of trauma and PTSD (McCarthy, 2008). Posttraumatic intrusions are represented by the “re-experiencing” subscale, which had good internal consistency in this sample (Cronbach's alpha ¼0.8). The Impact of Future Events Scale (IFES; Deeprose and Holmes, 2010) adapts the Impact of Events Scale (Horowitz, 1979) to measure the intrusiveness of imagery for prospective imagined events. Participants identify three future events (which can be negative or positive) and then respond to 24 items about their imagining of all three future events in the past week on a 0–4 scale (0 ¼“not at all”, 4 ¼“extremely”). For example “I thought about the future when I didn’t mean to”. The IFES produces a count of total reported positive versus negative future events from the three events reported by participants. A total intrusiveness score is calculated by summing responses for the 24 items about imagining future events (range¼0–96). The IFES is currently the only measure of prospective imagery available, and has been shown to have good test–retest reliability (r ¼0.73) and good internal consistency (Cronbach's alpha ¼0.93; Deeprose and Holmes, 2010), including in this sample (Cronbach's alpha ¼0.86). The Spontaneous Use of Imagery Scale (SUIS; Reisberg et al., 2003) is a 12-item measure of day-to-day non-affective imagery (e.g. “When I first hear a friend's voice, a visual image of him or her almost always springs to mind”). High scores indicate greater spontaneous use of day-to-day imagery. Mean scores for the SUIS were calculated to ensure that any group differences for intrusive prospective imagery could not be attributed to a systematic preference for use of imagery-based cognition in either group. The SUIS has good convergent validity with other measures of general non-affective imagery (Holmes et al., 2011). The SUIS had adequate internal consistency in the current sample (Cronbach's alpha ¼0.76).
between the HADS-A and IFES score, controlling for the influence of HADS-D, due to the common covariance of anxiety and depression.
3. Results 3.1. Summary statistics Demographic and clinical variables are presented in Table 1. The clinical group had completed significantly fewer years in education, and reported significantly higher total HADS, HADSA, and HADSD scores relative to controls. Of 25 patients, 48% scored above the threshold for probable PTSD as measured by the PDS. 5 patients did not provide sufficient data to conclude if they met criteria for PTSD or not. 3.2. Intrusive imagery analyses Patients with schizophrenia reported significantly greater intrusive imagery about future events than healthy controls, which remained significant after controlling for years of education (F (1,51) ¼20.44, p o0.001). As can be seen in Table 2, there was no difference between the groups for the number of negative future events identified, or in the general use of non-affective imagery. Within the clinical group there was a significant positive relationship between IFES and both HADSA scores (r ¼0.64, p4 0.001) and PDS re-experiencing symptoms (r ¼0.52, p ¼0.015). After controlling for HADS-D, there was still a significant relationship between HADS-A and IFES total (r¼ 0.43, p ¼0.001).
4. Discussion This is the first study to our knowledge to investigate prospective intrusive imagery in schizophrenia. As predicted, the patients with schizophrenia reported significantly greater intrusive prospective imagery relative to controls. Prospective intrusive imagery was associated with posttraumatic intrusions and Table 1 Socio-demographic and clinical characteristics. Clinical group (N ¼ 30)
Control group (N ¼ 27)
Test
Mean age (SD) in years
36.3 (8.1)
36.2 (8.5)
% Male
75
57.7
% White British
35.7
57.7
Mean (SD) years in education
14.1 (2.3)
16(2.3)
t(54)¼ 0.057, p¼ 0.95 X2 (1, N ¼54) ¼ 1.12, p ¼ 0.29 X2 (1, N ¼54) ¼ 1.81, p ¼ 0.18 t(54)¼ 3.03, p¼ 0.004
Clinical characteristics Mean (SD) HADS Total
11.8 (5.8)
8.1 (5.4)
Mean (SD) HADSA
6.6 (3.5)
4.8 (3.2)
Mean (SD) HADSD
5.2 (3.5)
3.4 (3.0)
% PTSD positive Mean (SD) PDS reexperiencing Mean (SD) PANSS total Mean (SD) PANSS-P Mean (SD) PANSS-N Mean (SD) PANSS-G
48 6.1 (4.1)
0 0.8 (1.3)
t(55)¼ 2.47, p¼ 0.017 t(55)¼ 2.098, p¼ 0.04 t(55)¼ 2.118, p¼ 0.04 n.a n.a
78.9 (18.1) 21.0 (6.8) 18.4 (6.8) 39.5 (9.9)
n.a n.a n.a n.a
n.a n.a n.a n.a
2.3. Data analysis All data were analysed in SPSS Statistics version 20 (IBM, 2011). The distributions for all variables met the assumptions for parametric tests. Means and percentages were calculated to describe clinical and control groups on socio-demographic and clinical descriptive variables. Univariate analyses were conducted to identify any group differences for clinical and socio-demographic variables. To address the first hypothesis, first, group mean differences were explored for the IFES intrusiveness and SUIS total scores using independent samples t tests. An analysis of covariance (ANCOVA) was carried out to control for possible confounding influence of years in education on IFES group differences. Second, the median number of negative future events reported by the clinical and control groups were compared using a Mann–Whitney U test. To address the second hypothesis, Pearson's correlational analyses were carried out using IFES total scores, HADSA total score and PDS re-experiencing subscale total. Bonferroni corrections were not applied as specific one-tailed a priori predictions had been made and all significant correlations were moderate to strong with highly significant associated alpha values (p o0.02). A secondary partial correlation was performed for the relationship
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Table 2 Group comparisons for IFES mean (SD) scores, median IFES negative events and SUIS mean (SD) scores. Clinical group Control group Test IFES mean (SD)
37.8 (12.6)
20.4 (11.8)
IFES median negative events SUIS mean (SD)
0
1
36.2 (9.5)
32.0 (9.5)
t(53)¼ 5.254, p o 0.001 z ¼ 0.53, p¼ 0.6 t(50)¼ 1.48, p ¼ 0.147
anxiety in schizophrenia. Importantly the patients did not report higher rates of general non-affective imagery compared to the healthy controls. These findings support the hypothesis that schizophrenia is associated with an abundance of intrusive imagery, but not a greater propensity to general non-affective imagery per se. Our findings are consistent with cognitive theory (e.g. Brewin et al., 2010) and make three important and novel contributions. Firstly, we found that patients with schizophrenia reported more intrusions about the future, as well as more retrospective intrusions, as predicted. Secondly, there was no significant group difference for the number of negative prospective events reported, suggesting that the intrusiveness of prospective imagery could not be attributed to the emotional valence of the future events reported (see also Jones and Steel, 2012, 2014). Thirdly, we found for the first time that prospective intrusive imagery was associated with posttraumatic intrusions from the past (i.e. re-experiencing symptoms). Taken together, these findings lend support to the idea that an underlying deficit such as weakened contextual integration, rather than an affective bias, may leave the individual vulnerable to experiencing, and indeed repeatedly re-experiencing, intrusions about the past and the future. Such vulnerability would leave one susceptible to both the symptoms of PTSD and the intrusions that are suspected to be the substance of hallucinations (Morrison, 2001). While the evidence is consistent with the notion of a contextual integration deficit in schizophrenia, the specific mechanism was not measured in this study and represents a common limitation. A specific and standardised measure of contextual integration has yet to be developed, but is crucial in establishing the relationship between contextual integration and intrusions. Typically, the focus of intrusions research has been in relation to negative retrospective events as it has developed out of research into PTSD – a diagnosis that depends upon a prior traumatic experience (Moulds and Holmes, 2011). Identifying that intrusions can occur in the absence of negative events opens up new avenues for research examining individual differences and vulnerabilities for intrusions, as well as developing our understanding of the mechanisms that underpin how we think about both the past and the future (e.g. Schacter et al., 2007). Intrusions for past events are central to cognitive models of psychosis (Morrison, 2001; Brewin et al., 2010). These models suggest that it is the appraisal of the intrusion that gives rise to, and maintains, psychotic phenomena. The current findings suggest that research should be extended to identify if appraisals of prospective imagery contribute to psychotic phenomena in the same way as for past events. Specifically in relation to Fowler et al. (2006) catastrophic interaction theory, it would be useful to identify if appraisals of prospective imagery are influenced by a sense of ongoing threat stemming from past trauma, and to distinguish prospective intrusions from apprehensions that a past trauma may reoccur. While there may be a shared vulnerability to intrusions for those who go on to develop PTSD or psychotic
symptoms, it is likely that it is the appraisal of the intrusion (e.g. appraising the intrusion as internally or externally generated) that determines the development of PTSD symptoms versus psychotic symptoms (e.g. Morrison, 2001), although this is yet to be explored. Similarly, it would be fruitful to specifically explore the relationship between intrusive prospective imagery and the presence and phenomenology of psychotic symptoms over time in a larger sample. Multidimensional measures have become increasingly popular in exploring the precise relationship between specific phenomena and the presence and phenomenology of psychotic symptoms (Steel et al., 2007) in ways that are not possible with conventional clinical measures such as the PANSS. In line with cognitive models of intrusions and psychosis it would be particularly useful to elucidate the relationship between anxiety, intrusive prospective imagery and frequency and distress of hallucinations and delusions in schizophrenia. Prospective intrusive imagery was associated with state anxiety in schizophrenia, even though individuals with schizophrenia did not report more negative future events. As discussed, it is possible that high rates of recalled trauma in the patients contributed to a sense of ongoing threat when thinking about the future, thereby heightening anxiety (e.g. Fowler et al., 2006). Further research would need to clarify this issue in a non-correlational design in order to better understand issues of causality. Regardless of the specific underlying mechanism, the association between prospective intrusive imagery and anxiety in schizophrenia suggests that prospective intrusive imagery may represent an important but as yet neglected treatment target. Further, if individuals with schizophrenia experience anxiety and intrusions when thinking about the future, they may respond with avoidance, thus hampering therapeutic work towards treatment goals. There has been a recent expansion in imagery-based cognitive-behavioural treatment protocols for a range of clinical presentations (e.g. Hackman et al., 2011). Such protocols may be fruitfully adapted to target prospective imagery in schizophrenia and other patient groups. Finally, although beyond the scope of the current paper, the current findings have some relevance for research into general non-affective imagery in schizophrenia, which has broadly attempted to identify whether there is a greater abundance or vividness of imagery in schizophrenia, particularly in relation to hallucinations (e.g. Chandiramani and Varma, 1987; Aleman et al., 2003; Sack et al., 2005), with inconsistent results. The findings in the present study suggest a specific elevation in the intrusiveness of imagery rather than an abundance of imagery in general. It may therefore be useful for future research to separate the intrusiveness of imagery to aid clearer analysis of vividness and frequency of general imagery in schizophrenia. In addition to the limitations discussed, it is also noted that this is a relatively small cross-sectional study. However, a priori power calculation indicated that the sample size was sufficient for the current analyses and it is hoped that the current findings may contribute to guiding larger scale longitudinal research. Further, it is also acknowledged that the current study would have benefitted from the addition of a clinical control group, specifically one with high levels of anxiety, to ensure that the current findings were unique to schizophrenia and not any clinical group. To conclude, the current study shows significantly elevated levels of intrusive prospective imagery in schizophrenia, and that within this sample intrusive prospective imagery was associated with posttraumatic intrusions and anxiety. The findings have important theoretical and clinical implications, particularly for the development of an information processing account of intrusions and psychotic phenomena in schizophrenia, and identify intrusive prospective imagery as a potentially important treatment target.
C.P. Malcolm et al. / Psychiatry Research 230 (2015) 899–904
Contributors CPM developed the study hypotheses and design, recruited participants and carried out the study, and wrote the present manuscript. MMP supervised the study design and recruitment of participants and commented on the final manuscript. LE supervised all aspects of the study and commented on the final manuscript.
Conflict of interest All authors declare they have no conflict of interest.
Role of funding source None.
Acknowledgements We thank all participants who took part in the study.
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Psychiatry Research journal homepage: www.elsevier.com/locate/psychres
Intrusive prospective imagery, posttraumatic intrusions and anxiety in schizophrenia Charlotte P. Malcolm a,n, Marco M. Picchioni b,c, Lyn Ellett a a
Department of Clinical Psychology, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK Institute of Psychiatry, King’s College, University of London, London SE5 8AF, UK c Academic Centre, St. Andrew’s, Cliftonville, Northampton NN1 5DG, UK b
art ic l e i nf o
a b s t r a c t
Article history: Received 29 March 2015 Received in revised form 30 September 2015 Accepted 17 November 2015 Available online 19 November 2015
Trauma exposure and intrusive thoughts are commonly reported in both schizophrenia and posttraumatic stress disorder (PTSD). Information processing accounts suggest that intrusions occur in the two conditions as a result of insufficient state and/or trait contextual processing in long-term memory. Most research has focused on intrusions about past events, while growing evidence suggests that intrusions about prospective imagined events warrants further investigation. Prospective intrusive imagery has yet to be examined in psychotic disorders but could provide crucial information regarding the aetiology and maintenance of psychotic symptoms. The current study examines the role of prospective intrusive imagery, posttraumatic intrusions and anxiety in schizophrenia. Fifty-seven participants (30 patients and 27 healthy controls) completed measures of trauma, PTSD, anxiety, general non-affective use of imagery, and intrusive prospective imagery. Patients reported significantly more intrusive prospective imagery relative to control participants but, importantly, not greater use of general non-affective imagery. Intrusive prospective imagery was associated with posttraumatic intrusions and anxiety in schizophrenia. The findings are consistent with information processing models of intrusions and psychosis, and provide novel insights for theoretical accounts, clinical formulation and therapeutic targets for psychotic symptoms in schizophrenia. & 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Psychosis PTSD Trauma Stress Hallucinations Cognition
1. Introduction A well-established link exists between trauma exposure and the development of schizophrenia (e.g. Bebbington et al., 2004; Bendall et al., 2010; van Os et al., 2010). Research finds varying rates of co-morbid PTSD in schizophrenia from around 13% to 53% (Mueser et al., 1998; Resnick et al., 2003; Howgego et al., 2005; Kilcommons and Morrison, 2005) with large differences in findings likely due to differing methodology (e.g. self-report versus clinical assessment; see Mueser et al., 2001) and the clinical context. However, the findings suggest higher rates of PTSD in schizophrenia than would be expected in the general populationaround 7.8–9.2% (Breslau et al., 1991; Kessler et al., 1995). Psychotic symptoms are also frequently and co-morbidly reported with PTSD (Anketell et al., 2010). However, the pathophysiological link between trauma and schizophrenia still remains unclear. To elucidate this link current research has explored common features and shared vulnerability factors for PTSD and schizophrenia. n
Corresponding author. E-mail address: [email protected] (C.P. Malcolm).
http://dx.doi.org/10.1016/j.psychres.2015.11.029 0165-1781/& 2015 Elsevier Ireland Ltd. All rights reserved.
Intrusive cognitions are a transdiagnostic feature of both PTSD and schizophrenia and may shed light on underlying cognitive mechanisms linking the two disorders. Intrusions are involuntary, unbidden cognitions, regarded as the “hallmark” of PTSD (Ehlers and Clark, 2000), but now considered to play a role in a range of other psychological disorders, including schizophrenia (Brewin et al., 2010; Morrison, 2001). Intrusions are believed to arise due to insufficient contextual integration during information processing and storage into long-term memory (Brewin, 2001; Brewin et al., 2010; Ehlers and Clark, 2000). Contextual integration, a function of the hippocampus, involves the processing and storage of autobiographical information with corresponding temporal and spatial information. Without adequate contextual processing, memory traces become disconnected from their temporal-spatial context; such that when the memory trace is triggered it intrudes into consciousness with a sense of “nowness” (Ehlers and Clark, 2000). During a traumatic event, information is processed rapidly via the amygdala with limited contextual integration, resulting in intrusions in the form of re-experiencing (e.g. “flashbacks”). For example, a year after an individual was involved in a terrifying car accident they may re-experience an intrusive image of the crash
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with a sense that it is happening in the present moment when they hear the screech of a car breaking. Cognitive models locate intrusions, and particularly the appraisal of intrusions, as central in the development and maintenance of psychotic phenomena (e.g. Morrison, 2001; Garety et al., 2001; Morrison et al., 2002; Read et al., 2005). Patients who experience positive psychotic symptoms are also more likely to report intrusions than other psychiatric and healthy control groups (Morrison and Baker, 2000; Morrison et al., 2002). Research has identified an attribution bias in individuals with psychosis whereby there is a tendency to attribute intrusions to external and malign sources (rather than internally generated memories) leading to emotional distress when intrusions are experienced (e.g. Bentall, 1990). The intrusion is then unwittingly maintained through maladaptive coping such as thought suppression or paranoid hypervigilence (Beck and Rector, 2003). Further, research (Steel et al., 2005; Fowler et al., 2006) has extended the cognitive models of memory processing (e.g. Brewin et al., 2010) to psychosis, identifying a “catastrophic interaction” between an underlying cognitive processing deficit and previous trauma in schizophrenia. Steel et al. (2005) cite evidence from experimental paradigms of context-dependent memory that baseline contextual processing is weaker in schizophrenia, conferring vulnerability to more frequent intrusions. Subsequent research has consistently found specific impairments in contextdependent memory and hippocampal function in schizophrenia, relative to non-context dependent memory, which remains intact (e.g. Weniger and Irle, 2008; Zierhut et al., 2010). Steel et al. (2005) further posit that past trauma results in emotional experiences that are insufficiently integrated in time and place, leading to a sense of current ongoing threat that influences the appraisal of intrusions. Intrusions from past long-term memory have received considerable theoretical attention (e.g. Ehlers and Clark, 2000; Brewin et al., 2010) but only provide a limited insight into the nature and consequences of intrusions. A large body of research over the past decade has provided consistent evidence that thinking about the future recruits the same cognitive processes and neural circuitry as remembering the past (see Szpunar et al., 2014 for a review), in part through the extraction and recombination of stored information to simulate a novel prospective event, leading to the concept of the “prospective brain” (Schacter et al., 2007). The concept of the prospective brain has led to an interesting line of research exploring how we can apply the vast body of knowledge of retrospective memory to understanding and enhancing cognition for future events (e.g. McLelland et al., 2014). Likewise, drawing on the concept of the prospective brain, Deeprose and Holmes (2010) have argued that intrusions about future events, specifically intrusive imagery, which exerts a stronger influence on emotions than verbal cognition (Beck, 1976), warrant further investigation. Historically it has been assumed that one must have already experienced an unpleasant event to experience intrusions for that event. Deeprose and Holmes (2010) have challenged that assumption, finding evidence that individuals report “flashforwards” or “pre-experiencing” of imagined future events, known as prospective intrusive imagery. Flashforwards exhibit the same phenomenological qualities as intrusive memories for past events: they are unbidden, involuntary and are accompanied by a sense of “nowness” (Holmes et al., 2007). Negative and distressing intrusions (e.g. a flashforward to the individual carrying out a suicidal act), maintain depression by perpetuating low mood (Deeprose and Holmes, 2010). Prospective intrusive imagery is associated with greater mood instability in bipolar disorder (Holmes et al., 2011) and greater state anxiety and depression in a range of affective disorders (Morina et al., 2011). There has been no work to date on prospective intrusive imagery in psychotic disorders but,
based on cognitive models of psychosis, it is expected that greater intrusive prospective imagery would be present in patients with schizophrenia. Anxiety is also common in schizophrenia (Braga et al., 2005) and exacerbates psychotic symptoms (Huppert and Smith, 2001). If present in schizophrenia, intrusive prospective imagery may similarly contribute to the positive symptoms and the elevated rates of anxiety in schizophrenia. The aims of this study were to investigate the presence of intrusive prospective imagery in schizophrenia relative to healthy controls, and identify the relationship between intrusive prospective imagery, retrospective intrusions and anxiety in schizophrenia. It was hypothesised that (1) individuals with schizophrenia will experience greater intrusive prospective imagery than controls, and (2) within the clinical group, prospective intrusive imagery will be positively associated with anxiety and retrospective intrusions in the form of posttraumatic re-experiencing.
2. Methods The research was approved by the London Stanmore (ref.: 12/ LO/0813) and Royal Holloway, University of London Psychology Department Ethics Committees (ref.: 2012/056). Patients completed measures in face-to-face interviews with the same researcher. Control participants completed measures in face-to-face interview format or as self-report measures depending on preference. 2.1. Participants Fifty-seven participants comprising patients (N ¼30; 22 male) and healthy controls (N ¼27; 16 male) were recruited. Sample size was determined by an a priori power calculation in line with Cohen's (1988) conventions to detect a large effect size (R2 40.05) in a correlational analysis, with alpha set at 0.05 and beta set at 0.2 (thus power is set at 0.8). The patients were formally diagnosed by a consultant psychiatrist with an ICD-10 (F20-21 and F25-25.9) schizophrenia spectrum disorder and recruited from 12 inpatient mental health wards in the south of England. All of the patients reported current positive symptoms, with most (N ¼26) reporting hallucinations. The control group was recruited through advertisements online and in public buildings. Participants were included if they were aged between 18 and 65 and provided written informed consent after a full description of the study. Patients were included if they had a diagnosis of a schizophrenia spectrum disorder. Exclusion criteria were history of significant head injury (loss of consciousness 45 min), neurological disorder or organic psychosis, current substance misuse, diagnosis of a personality disorder, poor comprehension of English, or an IQ of less than 70. Control participants were excluded if they reported a mental health diagnosis or symptoms of psychosis on the SCID IV psychosis screen (First et al., 1996). Control participants were excluded if they reported a trauma in addition to posttraumatic stress symptoms that constituted criteria for diagnosable PTSD as measured by the Posttraumatic Stress Diagnostic Scale (PDS; Foa, 1997). 2.2. Measures Hospital Anxiety and Depression Scale (HADS; Zigmond and Snaith, 1983): is a 14-item measure used to detect current symptoms of depression and anxiety and is a valid predictor of diagnosis and severity of depression and anxiety disorders (Bjelland et al., 2002). The HADS is composed of two subscales: HADS-A (7 items to detect anxiety) and HADS-D (7 items to detect depression). The HADS has good reliability for detecting anxiety and
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depression in schizophrenia (Allan and Martin, 2009). Positive and Negative Symptom Scale (PANSS; Kay, 1991) is the most widely used measure of symptoms of schizophrenia from the previous 72 h and is administered in interview format. The PANSS represents three separate subscales: positive, negative and general symptoms and has well-established reliability and validity (Kay et al., 2000). Posttraumatic stress diagnostic scale (PDS; Foa, 1997) is a selfreport measure of lifetime trauma type and posttraumatic symptom severity. The items reflect the DSM-IV diagnostic criteria for PTSD, including a subscale for re-experiencing, avoidance and arousal symptoms. The PDS is a valid and reliable measure of trauma and PTSD (McCarthy, 2008). Posttraumatic intrusions are represented by the “re-experiencing” subscale, which had good internal consistency in this sample (Cronbach's alpha ¼0.8). The Impact of Future Events Scale (IFES; Deeprose and Holmes, 2010) adapts the Impact of Events Scale (Horowitz, 1979) to measure the intrusiveness of imagery for prospective imagined events. Participants identify three future events (which can be negative or positive) and then respond to 24 items about their imagining of all three future events in the past week on a 0–4 scale (0 ¼“not at all”, 4 ¼“extremely”). For example “I thought about the future when I didn’t mean to”. The IFES produces a count of total reported positive versus negative future events from the three events reported by participants. A total intrusiveness score is calculated by summing responses for the 24 items about imagining future events (range¼0–96). The IFES is currently the only measure of prospective imagery available, and has been shown to have good test–retest reliability (r ¼0.73) and good internal consistency (Cronbach's alpha ¼0.93; Deeprose and Holmes, 2010), including in this sample (Cronbach's alpha ¼0.86). The Spontaneous Use of Imagery Scale (SUIS; Reisberg et al., 2003) is a 12-item measure of day-to-day non-affective imagery (e.g. “When I first hear a friend's voice, a visual image of him or her almost always springs to mind”). High scores indicate greater spontaneous use of day-to-day imagery. Mean scores for the SUIS were calculated to ensure that any group differences for intrusive prospective imagery could not be attributed to a systematic preference for use of imagery-based cognition in either group. The SUIS has good convergent validity with other measures of general non-affective imagery (Holmes et al., 2011). The SUIS had adequate internal consistency in the current sample (Cronbach's alpha ¼0.76).
between the HADS-A and IFES score, controlling for the influence of HADS-D, due to the common covariance of anxiety and depression.
3. Results 3.1. Summary statistics Demographic and clinical variables are presented in Table 1. The clinical group had completed significantly fewer years in education, and reported significantly higher total HADS, HADSA, and HADSD scores relative to controls. Of 25 patients, 48% scored above the threshold for probable PTSD as measured by the PDS. 5 patients did not provide sufficient data to conclude if they met criteria for PTSD or not. 3.2. Intrusive imagery analyses Patients with schizophrenia reported significantly greater intrusive imagery about future events than healthy controls, which remained significant after controlling for years of education (F (1,51) ¼20.44, p o0.001). As can be seen in Table 2, there was no difference between the groups for the number of negative future events identified, or in the general use of non-affective imagery. Within the clinical group there was a significant positive relationship between IFES and both HADSA scores (r ¼0.64, p4 0.001) and PDS re-experiencing symptoms (r ¼0.52, p ¼0.015). After controlling for HADS-D, there was still a significant relationship between HADS-A and IFES total (r¼ 0.43, p ¼0.001).
4. Discussion This is the first study to our knowledge to investigate prospective intrusive imagery in schizophrenia. As predicted, the patients with schizophrenia reported significantly greater intrusive prospective imagery relative to controls. Prospective intrusive imagery was associated with posttraumatic intrusions and Table 1 Socio-demographic and clinical characteristics. Clinical group (N ¼ 30)
Control group (N ¼ 27)
Test
Mean age (SD) in years
36.3 (8.1)
36.2 (8.5)
% Male
75
57.7
% White British
35.7
57.7
Mean (SD) years in education
14.1 (2.3)
16(2.3)
t(54)¼ 0.057, p¼ 0.95 X2 (1, N ¼54) ¼ 1.12, p ¼ 0.29 X2 (1, N ¼54) ¼ 1.81, p ¼ 0.18 t(54)¼ 3.03, p¼ 0.004
Clinical characteristics Mean (SD) HADS Total
11.8 (5.8)
8.1 (5.4)
Mean (SD) HADSA
6.6 (3.5)
4.8 (3.2)
Mean (SD) HADSD
5.2 (3.5)
3.4 (3.0)
% PTSD positive Mean (SD) PDS reexperiencing Mean (SD) PANSS total Mean (SD) PANSS-P Mean (SD) PANSS-N Mean (SD) PANSS-G
48 6.1 (4.1)
0 0.8 (1.3)
t(55)¼ 2.47, p¼ 0.017 t(55)¼ 2.098, p¼ 0.04 t(55)¼ 2.118, p¼ 0.04 n.a n.a
78.9 (18.1) 21.0 (6.8) 18.4 (6.8) 39.5 (9.9)
n.a n.a n.a n.a
n.a n.a n.a n.a
2.3. Data analysis All data were analysed in SPSS Statistics version 20 (IBM, 2011). The distributions for all variables met the assumptions for parametric tests. Means and percentages were calculated to describe clinical and control groups on socio-demographic and clinical descriptive variables. Univariate analyses were conducted to identify any group differences for clinical and socio-demographic variables. To address the first hypothesis, first, group mean differences were explored for the IFES intrusiveness and SUIS total scores using independent samples t tests. An analysis of covariance (ANCOVA) was carried out to control for possible confounding influence of years in education on IFES group differences. Second, the median number of negative future events reported by the clinical and control groups were compared using a Mann–Whitney U test. To address the second hypothesis, Pearson's correlational analyses were carried out using IFES total scores, HADSA total score and PDS re-experiencing subscale total. Bonferroni corrections were not applied as specific one-tailed a priori predictions had been made and all significant correlations were moderate to strong with highly significant associated alpha values (p o0.02). A secondary partial correlation was performed for the relationship
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Table 2 Group comparisons for IFES mean (SD) scores, median IFES negative events and SUIS mean (SD) scores. Clinical group Control group Test IFES mean (SD)
37.8 (12.6)
20.4 (11.8)
IFES median negative events SUIS mean (SD)
0
1
36.2 (9.5)
32.0 (9.5)
t(53)¼ 5.254, p o 0.001 z ¼ 0.53, p¼ 0.6 t(50)¼ 1.48, p ¼ 0.147
anxiety in schizophrenia. Importantly the patients did not report higher rates of general non-affective imagery compared to the healthy controls. These findings support the hypothesis that schizophrenia is associated with an abundance of intrusive imagery, but not a greater propensity to general non-affective imagery per se. Our findings are consistent with cognitive theory (e.g. Brewin et al., 2010) and make three important and novel contributions. Firstly, we found that patients with schizophrenia reported more intrusions about the future, as well as more retrospective intrusions, as predicted. Secondly, there was no significant group difference for the number of negative prospective events reported, suggesting that the intrusiveness of prospective imagery could not be attributed to the emotional valence of the future events reported (see also Jones and Steel, 2012, 2014). Thirdly, we found for the first time that prospective intrusive imagery was associated with posttraumatic intrusions from the past (i.e. re-experiencing symptoms). Taken together, these findings lend support to the idea that an underlying deficit such as weakened contextual integration, rather than an affective bias, may leave the individual vulnerable to experiencing, and indeed repeatedly re-experiencing, intrusions about the past and the future. Such vulnerability would leave one susceptible to both the symptoms of PTSD and the intrusions that are suspected to be the substance of hallucinations (Morrison, 2001). While the evidence is consistent with the notion of a contextual integration deficit in schizophrenia, the specific mechanism was not measured in this study and represents a common limitation. A specific and standardised measure of contextual integration has yet to be developed, but is crucial in establishing the relationship between contextual integration and intrusions. Typically, the focus of intrusions research has been in relation to negative retrospective events as it has developed out of research into PTSD – a diagnosis that depends upon a prior traumatic experience (Moulds and Holmes, 2011). Identifying that intrusions can occur in the absence of negative events opens up new avenues for research examining individual differences and vulnerabilities for intrusions, as well as developing our understanding of the mechanisms that underpin how we think about both the past and the future (e.g. Schacter et al., 2007). Intrusions for past events are central to cognitive models of psychosis (Morrison, 2001; Brewin et al., 2010). These models suggest that it is the appraisal of the intrusion that gives rise to, and maintains, psychotic phenomena. The current findings suggest that research should be extended to identify if appraisals of prospective imagery contribute to psychotic phenomena in the same way as for past events. Specifically in relation to Fowler et al. (2006) catastrophic interaction theory, it would be useful to identify if appraisals of prospective imagery are influenced by a sense of ongoing threat stemming from past trauma, and to distinguish prospective intrusions from apprehensions that a past trauma may reoccur. While there may be a shared vulnerability to intrusions for those who go on to develop PTSD or psychotic
symptoms, it is likely that it is the appraisal of the intrusion (e.g. appraising the intrusion as internally or externally generated) that determines the development of PTSD symptoms versus psychotic symptoms (e.g. Morrison, 2001), although this is yet to be explored. Similarly, it would be fruitful to specifically explore the relationship between intrusive prospective imagery and the presence and phenomenology of psychotic symptoms over time in a larger sample. Multidimensional measures have become increasingly popular in exploring the precise relationship between specific phenomena and the presence and phenomenology of psychotic symptoms (Steel et al., 2007) in ways that are not possible with conventional clinical measures such as the PANSS. In line with cognitive models of intrusions and psychosis it would be particularly useful to elucidate the relationship between anxiety, intrusive prospective imagery and frequency and distress of hallucinations and delusions in schizophrenia. Prospective intrusive imagery was associated with state anxiety in schizophrenia, even though individuals with schizophrenia did not report more negative future events. As discussed, it is possible that high rates of recalled trauma in the patients contributed to a sense of ongoing threat when thinking about the future, thereby heightening anxiety (e.g. Fowler et al., 2006). Further research would need to clarify this issue in a non-correlational design in order to better understand issues of causality. Regardless of the specific underlying mechanism, the association between prospective intrusive imagery and anxiety in schizophrenia suggests that prospective intrusive imagery may represent an important but as yet neglected treatment target. Further, if individuals with schizophrenia experience anxiety and intrusions when thinking about the future, they may respond with avoidance, thus hampering therapeutic work towards treatment goals. There has been a recent expansion in imagery-based cognitive-behavioural treatment protocols for a range of clinical presentations (e.g. Hackman et al., 2011). Such protocols may be fruitfully adapted to target prospective imagery in schizophrenia and other patient groups. Finally, although beyond the scope of the current paper, the current findings have some relevance for research into general non-affective imagery in schizophrenia, which has broadly attempted to identify whether there is a greater abundance or vividness of imagery in schizophrenia, particularly in relation to hallucinations (e.g. Chandiramani and Varma, 1987; Aleman et al., 2003; Sack et al., 2005), with inconsistent results. The findings in the present study suggest a specific elevation in the intrusiveness of imagery rather than an abundance of imagery in general. It may therefore be useful for future research to separate the intrusiveness of imagery to aid clearer analysis of vividness and frequency of general imagery in schizophrenia. In addition to the limitations discussed, it is also noted that this is a relatively small cross-sectional study. However, a priori power calculation indicated that the sample size was sufficient for the current analyses and it is hoped that the current findings may contribute to guiding larger scale longitudinal research. Further, it is also acknowledged that the current study would have benefitted from the addition of a clinical control group, specifically one with high levels of anxiety, to ensure that the current findings were unique to schizophrenia and not any clinical group. To conclude, the current study shows significantly elevated levels of intrusive prospective imagery in schizophrenia, and that within this sample intrusive prospective imagery was associated with posttraumatic intrusions and anxiety. The findings have important theoretical and clinical implications, particularly for the development of an information processing account of intrusions and psychotic phenomena in schizophrenia, and identify intrusive prospective imagery as a potentially important treatment target.
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Contributors CPM developed the study hypotheses and design, recruited participants and carried out the study, and wrote the present manuscript. MMP supervised the study design and recruitment of participants and commented on the final manuscript. LE supervised all aspects of the study and commented on the final manuscript.
Conflict of interest All authors declare they have no conflict of interest.
Role of funding source None.
Acknowledgements We thank all participants who took part in the study.
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