ORIGINAL ARTICLE

Emotional Behavior in Acute Stroke

The Lausanne Emotion in Stroke Study
Selma Aybek, MD,* Antonio Carota, MD,* Florence Ghika-Schmid, MD,* Alexandre Berney, MD, Guy Van Melle, PhD, Patrice Guex, MD, and Julien Bogousslavsky, MD*
Key Words: emotion, acute stroke, scale, behavior, assessment

Objective: To study emotional behaviors in an acute stroke

population.

(Cog Behav Neurol 2005;18:3744)

Background: Alterations in emotional behavior after stroke have been recently recognized, but little attention has been paid to these changes in the very acute phase of stroke. Methods: Adult patients presenting with acute stroke were prospectively recruited and studied. We validated the Emotional Behavior Index (EBI), a 38-item scale designed to evaluate behavioral aspects of sadness, aggressiveness, disinhibition, adaptation, passivity, indifference, and denial. Clinical, historical, and imaging (computed tomography/magnetic resonance imaging) data were obtained on each subject through our Stroke Registry. Statistical analysis was performed with both univariate and multivariate tests. Results: Of the 254 patients, 40% showed sadness, 49% passivity,
17% aggressiveness, 53% indifference, 76% disinhibition, 18% lack of adaptation, and 44% denial reactions. Several signicant correlations were identied. Sadness was correlated with a personal history of alcohol abuse (r = P , 0.037), female gender (r = P , 0.028), and hemorrhagic nature of the stroke (r = P , 0.063). Aggressiveness was correlated with a personal history of depression (r = P , 0.046) and hemorrhage (r = P , 0.06). Denial was correlated with male gender (r = P , 0.035) and hemorrhagic lesions (r = P , 0.05). Emotional behavior did not correlate with either neurologic impairment or lesion localization, but there was an association between hemorrhage and aggressive behavior (P , 0.001), lack of adaptation (r = P , 0.015), indifference (r = P , 0.018), and denial (r = P , 0.045).

Conclusions: Systematic observations of acute emotional behaviors after stroke suggest that emotional alterations are independent of mood and physical status and should be considered as a separate consequence of stroke.

Received for publication September 30, 2004; accepted November 18, 2004. *Department of Neurology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; Service of Liaison Psychiatry, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; and University Institute of Social and Preventive Medicine, Lausanne, Switzerland. This work was supported by Swiss National Research Foundation grants 32-41950-94, 3200-050728-97, and 3200-061342-00/1. Reprints: Dr. Julien Bogousslavsky, Service de Neurologie, Centre Hospitalier Universitaire Vaudois, 1011 Lausanne, Switzerland (e-mail: Julien. Bogousslavsky@chuv.hospvd.ch). Copyright 2005 by Lippincott Williams & Wilkins

otor, sensory, and cognitive decits are classically recognized as clinical signs of a stroke. It is only during the 20th century that modications of affective and emotional behavior have been recognized in cerebrovascular diseases, with Kraeplin1 (1921) rst describing an association between depression and atherosclerotic diseases. Later, Goldstein2 (1948) described the catastrophic reaction observed in braininjured patients, and Gainotti3 (1972) conducted the rst systematic study of emotional symptoms associated with cerebrovascular lesions. Since then, poststroke behavioral changes have drawn much attention but have been studied mainly during the chronic phase of stroke.46 As with all the other clinical manifestations of stroke, emotional symptoms can evolve very quickly, and their study in the acute phase of stroke is of great interest for management and outcome of illness. Several scales have been developed with a special emphasis on reporting and quantifying mood and behavior changes after stroke,7,8 but an adequate tool in the acute setting does not exist. The study of emotion in stroke patients is particularly difcult because the variables involved are multiple and complex. One problem is the denition of emotion itself, as it can be expressed in three main ways9: 1. A subjective feeling or state experienced by the patient, for example, happiness, sadness, fear, anger, disgust, or surprise. 2. Physiologic reactions characterized by somatic visceral autonomic responses, for example, increased heart rate, blood pressure, salivation, or perspiration. 3. A behavioral component that can be observed, for example, running away when afraid or smiling when happy. When trying to apply those denitions to design a study protocol for stroke patients, we are confronted with the difculty of the clinical interpretation of subjective experience, which shows large interpatient and time variation and requires generally intact speech and language abilities. Patients with language impairment are often not able to verbalize their emotional experiences and cannot be interviewed in a reliable manner,10 requiring some form of language-independent analysis. Furthermore, the study of physiologic components (pulse, heart rate, skin conductance response),11,12 although possible, requires equipment and approaches that are not readily applicable to a large cohort of patients during the very

Cog Behav Neurol  Volume 18, Number 1, March 2005

37

Aybek et al

Cog Behav Neurol  Volume 18, Number 1, March 2005

acute phase of stroke when the patients are in a critical state. Also, the specicity of these ndings is questionable, as stroke patients can develop somatic and visceralautonomic changes without concomitant emotional changes. An approach that appears more feasible for clinical research into emotions in a stroke population is to focus on the third aspect of emotions: displayed behavior. To address this need, we chose to create a new computed database, based on an observational model, to survey and study a broad range of emotional behaviors of stroke patients during the rst days following stroke. The interest of such a study lies in anatomicclinical correlations between emotional behavior and lesion topography and the potential recognition of early markers during the acute phase of stroke, which could be used subsequently to assess the development of affective disorders.13

TABLE 1. Emotional Behavior Index Form

Sadness Cries Looks sad Complains Screams Groans Passivity Gives up Isolated Aggressiveness Tense Agitated Angry Rebellious Opposed Aggressive Revolted Indifference Indifferent Neglected Apathetic Disinhibition Jokes Disinhibited Laughs Impatient Denial Minimizes Total denial Partial denial Adaptation Smiles Sociable Quiet Patient Capable of founded request Decent Interested, curious Looks serious Interactive Accommodating Helpful Expressive Tidy Docile

METHODS Participants
Patients presenting with a rst-ever stroke and admitted within 24 hours of onset to our acute care unit between 1995 and 1999 were enrolled for prospective study. We excluded patients whose nal diagnosis was transient ischemic attack (TIA). The inclusion criteria used were those for the Lausanne Stroke Registry (LSR),14 to allow direct comparison of our emotional data with the LSR epidemiologic data (age, sex, race, smoking, previous TIA, and cardiovascular risk factors), radiologic data (volume and lesion localization according to templates from computed tomography [CT] or magnetic resonance imaging [MRI] examination), and neurologic data (stroke type, stroke etiology, and degree of motor, sensory, and cognitive decit).

using the scale, the nurses underwent uniform training in how to complete the EBI to increase the reliability of the measure.

Clinical Data
Evaluations were made by the medical investigator over the rst 7 days following the stroke. To assess signs of denial, we queried participants about their recollection of the stroke event (adequate, partial, or absent) and whether they sought medical care or were brought to medical attention by another person.13,18 A subjective appreciation was obtained of the patients feelings such as happiness, sadness, anger, and fear. We also looked for other emotional behaviors19 not tested on our scale, such as catastrophic reaction20 (disruptive emotional outburst involving anxiety, agitation, and aggressive behavior when the patient is confronted with a task he/she is unable to perform because of his/her neurologic decit), emotionalism21 (crying or laughing with little or no warning in response to a meaningful trigger stimulus and accompanied by a corresponding affect), pathologic laughing and crying22 (in response to a trigger stimulus of no importance with no corresponding affect), and loss of self-activation23 (apathy, indifference, lack of motivation, aspontaneity, and inability to undertake any kind of activity) and abulia24 (at affect, delayed answers, reduced motor response, hypophonia, and xed gaze). Mood status was evaluated using the Hamilton Depression/Anxiety Rating Scales,25 a score of $8 more being interpreted as the presence of depressive/anxiety signs. We systematically looked for diagnostic confounders of depression (Table 2), such as feeding and sleep disturbances, confusional state, connement to bed, and immobility, which are frequent in hospitalized patients and can be misinterpreted as apathy in stroke patients. Cognitive and behavioral examination was performed by a clinical neuropsychologist using the Mini-Mental State Examination26 together with our locally developed screening battery,27 which includes an evaluation of multiple cognitive domains but from which we extracted the data concerning aphasia, apraxia, and anosognosia. Speech
q 2005 Lippincott Williams & Wilkins

Procedures Emotional Behavior Index

All patients were examined using a specically designed observational scale, the Emotional Behavior Index (EBI). The 38 items composing the EBI correspond to the problematic emotional behaviors most frequently observed after stroke,3,15,16 grouped into the seven categories of sadness, passivity, aggressiveness, indifference, disinhibition signs, adaptation, and denial (Table 1). The EBI is an ordinal scale containing a score for each category over 4 days of observation. The item was considered positive when it reected the observed behavior throughout the whole day (score = 1). We then considered the emotional behavior (grouped items) to be present if the mean score was $1 (sum of all the items observed in one category for the 4 days, divided by the number of items in this category). As the EBI is a new tool, we conducted a preliminary study17 to establish certain psychometric attributes. To test the interrater reliability, two experienced nurses independently completed the EBI for each study participant, blinded to the others evaluation. We were not able to study the testretest reliability because the behavior was changing every day, but we tested the interitem reliability for each category, with the item-total correlation (each item was correlated to the sum of the item of the category). Before

38

Cog Behav Neurol  Volume 18, Number 1, March 2005

Emotional Behavior in Acute Stroke

TABLE 2. Diagnostic Confounders of Depressive Syndrome After Stroke

Indirect Common to many severely ill, hospitalized patients Controlled appetite (e.g., NPO, tube feeding) Awakened frequently Aphasia Direct

TABLE 3. Reliability of the Emotional Behavior Index

Category Sadness R 0.72 Item Cries Looks sad Complains Screams Tense Agitated Angry Rebellious Opposed Aggressive Revolted Gives up Isolated Indifferent Neglected Apathetic Jokes Disinhibited Laughs Impatient Minimizes Total denial Partial denial Smiles Sociable Quiet Patient Capable of request Decent Curious Looks serious Interactive Accommodating Helpful Expressive Tidy Docile r 0.41 0.52 0.35 0.37 0.35 0.38 0.40 0.55 0.50 0.60 0.48 0.50 0.30 0.43 0.44 0.46 0.45 0.55 0.47 0.32 0.46 0.54 0.55 0.43 0.55 0.53 0.43 0.38 0.38 0.53 0.47 0.45 0.34 0.32 0.43 0.35 0.46

Amnesia/cognitive impairment Anosognosia/denial of depression Conned to bed Aprosody Delirium (acute confusional states) Apathy syndromes Of special concern in stroke patients Isolated abulia/apathy Immobility (potential confusion with apathy) Loss of self activation Dysphagia (interferes with eating habits) Frontal lobe syndrome Slurred speech (and resultant miscommunication) KluverBucy syndrome Korsakoff syndrome Fatigue Special behavioral syndromes Emotionalism Catastrophic reaction

Aggressiveness

0.91

Passivity Indifference

0.70 0.79

Disinhibition

0.59

Denial

0.68

disturbances were classied as motor aphasia, sensory aphasia, or global aphasia. Patients with constructive and/or ideomotor apraxia were identied as well as patients with buccolingofacial apraxia. Anosognosia was examined according to the established criteria of Bisiach et al.28 Complete neurologic examination was performed and recorded according to the items of the LSR. Lesion analysis was performed by CT and/or MRI examination. All patients had a CT scan on admission; when the lesion was not visualized on the rst image, CT or MRI (T1, T2, and diffusion weighted) was performed at 24 hours. A neuroradiologist, blinded to the clinical ndings, interpreted images and classied lesions according to their supra/infratentorial, right/left/bilateral, cortical/subcortical, and anterior/posterior location with reference to our locally developed templates,29,30 but the size of the lesion was not taken into account in this study.

Adaptation

0.89

R = interrater correlation coefcient (.0.50); r = interitem correlation coefcient (.0.30).

Statistical Analysis
Discrete variables were analyzed with Fisher exact test. Variables found to be signicant using the univariate approach were entered in the multivariate logistic regression and tested stepwise (step down) at a signicance level of 0.10.

Emotional Behavior in Acute Stroke Epidemiologic Data

A total of 326 patients were enrolled in the study. When analyzing the data, we determined that some data were missing for 72 patients. That is, complete days of evaluation were missing, owing to premature transfer of the patient from the acute care unit either to the general care unit or to another department for medical reasons. We therefore analyzed the data from 254 patients assessed for 3 or 4 days using the EBI. To determine if this resulted in a bias, we compared our patients with the total stroke population of the registry and found them to be comparable in terms of epidemiologic (sex, hypertension, diabetes, smoking, cholesterol, oral contraceptives,

RESULTS Reliability of EBI

The preliminary study17 involved 35 patients (17 men and 18 women) with a mean age of 70.3 years. This population was identical in terms of epidemiologic and medical data to the overall stroke registry population. The interrater reliability showed acceptable to good values for each of the seven categories, as did the interitem reliability (Table 3).
q 2005 Lippincott Williams & Wilkins

39

Aybek et al

Cog Behav Neurol  Volume 18, Number 1, March 2005

migraine, family history, cardiac ischemia, arrhythmia, claudication, previous TIA, and presumed cause of stroke) and clinical characteristics. We therefore assumed our population to be representative of a general stroke population. The 254 patients consisted of 136 males and 118 females, with a mean age of 64.8 years. Fifty-one percent had a right lesion, 45% a left lesion, and 4% a bilateral lesion. The lesion was anterior in 58%, posterior in 42%, cortical in 37%, and subcortical in 63%. Ninety-ve percent of lesions were ischemic and 5% hemorrhagic, whereas 20% were infratentorial lesions and 80% supratentorial (Table 4).

Global Results
Forty percent of patients showed sadness, 49% passivity, 17% aggressiveness, 53% indifference, 76% disinhibition signs, 18% lack of adaptation, and 44% denial reactions (Fig. 1). Ten percent of patients had no recall of the acute event, 24% had partial recall, and 66% had adequate recall. Fifty-two percent of patients sought medical care by themselves, whereas 48% had to be brought to medical attention by a third party. Patients with total recall of the event presented fewer denial signs (34%) than patients with partial (60%) or no (66%) recall (P , 0.01). Patients with no recall displayed a higher frequency of indifference (67%) than patients with total recall (39%) (P , 0.02). Eighty-eight percent of patients showing signs of adaptation had total recall of the event (P , 0.009). When correlating the different categories of emotional behaviors, we found that they were independent, except for sadness, which seemed to be associated with aggressiveness (seen in 30% of aggressive patients and 10% of nonaggressive patients) (P , 0.001) and indifference (seen in 65% of indifferent patients and 44% of nonindifferent patients) (P , 0.001). Aggressive patients also showed a higher frequency of denial signs (66%) than nonaggressive patients (40%) (P , 0.005).

FIGURE 1. The x axis denotes the seven categories of emotions in the Emotional Behavior Index; the y axis denotes the percentages of patients presenting the emotions.

Gender and Emotions

The EBI showed that women were signicantly more prone to showing signs of sadness than men (46% and 35%, respectively) (P , 0.04) and women described themselves as being sad (56%) more often than men (43%) (P , 0.04). The subjective feeling seemed to correlate with the observed behavior, since, of the patients describing themselves as not feeling sad, 71% were judged as not sad by the EBI and 29% were judged sad (P , 0.04).

Women also more often described a subjective feeling of anger (63%) and fear (63%) than men (both 37% in men) (P , 0.04 and P , 0.01, respectively). Men more frequently showed denial signs than women (49% vs 37%) (P , 0.04).

Subjective Experiences and Emotions

In terms of patients subjective experiences, we found that 65% expressed joy, 38% sadness, 15% disgust, 17% anger, and 24% fear. Apart from the interaction between the subjective feeling of sadness and observed sadness described above, no interactions were found between subjective feelings and the EBI score.

TABLE 4. Type and Location of Lesions

Type of stroke Laterality of lesion Anterior/posterior pole Cortical/subcortical lesion Supra/infratentorial lesion 5% hemorrhagic 51% right 11% anterior 24% cortical 95% ischemic 45% left 15% posterior 35% subcortical 4% bilateral

Affective Disorders and Emotions

Almost 15% of patients had a history of previous depressive disorders, and 10% had a positive family history of depressive disorders. Twenty-ve percent of patients with a personal history of depression showed aggressive signs compared with only 10% of patients with no history of depression (P , 0.03). No correlation was found between a history of previous psychiatric disorders (other than depression) and the EBI score. Sadness correlated with a history of
q 2005 Lippincott Williams & Wilkins

80% supratentorial 20% infratentorial

40

Cog Behav Neurol  Volume 18, Number 1, March 2005

Emotional Behavior in Acute Stroke

alcohol abuse, as it was expressed by 83% and 35%, respectively, of patients with and without a history of alcohol abuse (P , 0.025). A family history of depression, psychiatric disorders, or alcohol abuse did not inuence emotional behavior. Twenty percent of our patients presented a Hamilton Depression score of $8, showing some degree of depression. We failed to demonstrate any correlation with the EBI, apart from the sadness category (P , 0.005). On the Hamilton Anxiety Scale, 7% of patients had a score of .8, showing some degree of anxiety, but again there was no correlation with the EBI score. No gender difference was noticed in terms of the Hamilton Depression and Anxiety Scales.

entities were independent of the epidemiologic data, the EBI, and lesion characteristics except for abulia, in which we found a higher frequency of hemorrhagic lesions (P , 0.001).

Multivariate Analysis
All of the relevant variables were entered in a multivariate logistic regression model. Sadness was correlated with a personal history of alcohol abuse (P , 0.037), female gender (P , 0.028), and hemorrhagic nature of the stroke (P , 0.063). Aggressiveness was correlated with a personal history of depression (P , 0.046) and hemorrhagic lesions (P , 0.06). Denial was correlated to the male gender (P , 0.035) and hemorrhagic lesions (P , 0.05). As most of the emotional behavior seemed to correlate with hemorrhagic lesions in the univariate analysis, we built a global emotional score (sum of the categories presented by one patient), which we considered to be positive if at least two emotional behaviors of seven were present. The correlation of this score with hemorrhagic lesions did not reach signicance.

Lesion Characteristics and Emotions

Each category of the EBI was correlated to the side of the lesion, its anterior/posterior pole, and cortical/subcortical localization, but no signicant association was determined. The only correlation found was that disinhibition was more often expressed in cases with supratentorial lesions (P , 0.001). When the EBI score was compared with stroke type, an association was found between hemorrhagic lesions and expression of indifference (P , 0.018), aggressive behavior (P , 0.001), lack of adaptation (P , 0.015), and denial signs (P , 0.045).

DISCUSSION EBI
There have been few studies testing emotional behaviors in large samples of patients, especially in the acute phase of stroke. We created a tool to evaluate emotional behaviors and rst had to validate it concerning its psychometrics attributes,31 validity, and reliability. The validity of a new measurement tool is usually appreciated with the face validity and construct validity. The second entity was difcult to obtain as no other scales measuring observed behaviors in the acute phase of stroke exist, and we were then unable to conduct statistical analysis. However, our clinical experience, supported by other validated works,16 allowed us to accept the face validity of the EBIs items to be sufcient. Then again, we tested the interrater and interitem reliability of our observational form, which gave good results. We can then assume that the EBI can be easily applied by any observer. However, the evaluation should be made by a person who is able to spend time with the patient, a condition that was met in our study, since the EBI was completed by nurses who were present in the acute care unit for the whole day. The EBI is therefore a tool that should be used under suitable conditions. The patients included in our study showed epidemiologic data representative of a general stroke population. This

Clinical Manifestation of Stroke and Emotions

The EBI score did not correlate with the type or degree of motor and sensory decit (Table 5). The correlation between the EBI score and cognitive decits (see Table 5) showed that aphasic patients had signicantly more frequent signs of passivity (59%) than nonaphasic patients (43%) (P , 0.023), but the two groups did not differ in terms of other emotional behaviors. Apraxic patients (76%) also showed passivity more frequently than nonapraxic patients (44%) (P , 0.001), but there were no differences in the other EBI parameters. As shown in Figure 2, compared with patients without anosognosia, patients with anosognosia showed a higher frequency of sadness (P , 0.001), passivity (P , 0.007), aggressiveness (P , 0.019), indifference (P , 0.001), and denial (P , 0.026).

Other Pseudo-Depressive Mood Disorders

Eighteen percent of our patients showed abulia, 8% loss of self-activation, 0.16% pathologic laughing and crying, 7% emotionalism, and 0.5% catastrophic reactions. All those

TABLE 5. Neurologic and Cognitive Examination

Aphasia 69% 12% 10% 9% absent global motor sensory Apraxia 81% absent 14% ideomotor and/or constructive 5% buccolinguofacial Anosognosia 87.6% absent 13.4% anosognosia Neurologic Decit 17% pure motor 3% pure sensory 30% motor + sensory 1.7% motor + visual eld 0.3% sensory + visual eld 17% motor + sensory + visual eld 3% pure visual eld 28% other

q 2005 Lippincott Williams & Wilkins

41

Aybek et al

Cog Behav Neurol  Volume 18, Number 1, March 2005

Emotional Behaviors and Brain Lesions Adaptation and Disinhibition

When emotional behavior during the acute phase of stroke was examined, most of the patients showed good adaptation, although many showed some signs of disinhibition (76%). This result cannot be compared with other ndings in the literature, as no precise epidemiologic studies of disinhibition have been reported. In terms of anatomicclinical correlates, the only correlation found was that disinhibition was signicantly associated with supratentorial lesions. In contrast to other authors,38 we did not nd any differences between right and left hemisphere localization; this may be explained by the fact that we considered only three of the ve aspects of disinhibition syndrome described by these authors (motor, instinctive, emotional, intellectual, and sensory). We chose to restrict our evaluation to motor (eg, hyperactivity), instinctive (eg, hypersexuality and hyperphagia), and emotional (eg, euphoria and elation) aspects and omitted intellectual (eg, ight of ideas) and sensory (eg, hallucinations) aspects, because these depend on speech ability. Here again, we are confronted with the difculties encountered when trying to study emotions, especially concerning language-dependent measures.35

FIGURE 2. The x axis denotes emotional behaviors; the y axis denotes the percentages of patients showing the emotional behaviors. (Light columns), patients with anosognosia; (dark columns), patients without anosognosia.

Aggressiveness
When looking at aggressive behavior, we did not nd any right/left, cortico/subcortical, supra/infratentorial, or anterior/posterior location and were not able to conrm a precise localization as did some authors concerning nondirected aggressiveness (associated with lesions of the hypothalamus,39,40 caused by bilateral destruction of the ventromedial hypothalamic area by a tumor) and directed aggressiveness (associated with cortical lesions, as reported in a study41 on patients with orbitofrontal cortex lesions, who displayed increased expression of aggressive feelings to trivial stimuli). However, an interesting nding is that patients with hemorrhagic lesions in our study had a tendency to show aggressive behavior more often, a fact that has not been reported in the literature. The interactions between the complex mechanisms leading to aggressive behavior remain to be investigated, as we still do not know whether pathologic aggression is primarily organic or functional (consequence of psychologic sequelae).41

allowed us to avoid one of the biggest biases described in the literature, namely, the exclusion of patients with severe cognitive impairment or aphasia. Robinson et al,3234 who found an effect of localization on poststroke depression, discussed this issue and stated that the exclusion of aphasic patients did not signicantly modify the results. However, Gainotti et al35 found that when recording patients who could not be assessed or could be evaluated only using nonverbal mood measurements, the localization of the lesion was not signicant. This controversy relates to the measurement of depression, but the same methodologic issues are encountered for emotional behaviors. It is not always easy to make a clear distinction between emotions and affective disorders in the existing literature. The terminology used by certain authors when discussing affective disorders, mood disturbance, psychological impact of stroke, or emotion is not always precise. In our study, we clearly dened emotional behaviors with the use of a scale. We also made a precise distinction between emotional behavior (tested using the EBI), depression (Hamilton scale), and other pseudo-depressive disorders that should not be confounded with depression, such as catastrophic reactions, pathologic laughing and crying, apathy, emotionalism, and loss of psychic self-activation.19 As these are difcult to diagnose, they may have been included in other clinical descriptions, and this may explain some of the discrepancies in the results of a number of studies on affective disorders following stroke.33,36,37 The fact that our computerized database containing the EBI data is compatible with our neurologic database (LSR) also allows us to make precise correlations, especially concerning localization of stroke.

Indifference and Passivity

As regards indifference behavior, described as being more frequent in right hemispheric lesions,15 we found a higher percentage of right lesions (52%) than left lesions (48%), but the difference did not reach statistical signicance. De Agostini et al16 obtained conicting results and supported the idea that indifference was probably noted in patients with a right lesion under test conditions but not when observed in an objective manner outside the context of the test. This theory is supported by our results obtained under the same conditions.

Denial
We did not nd any signicant anatomic correlation for denial. There are many etiologic theories for this disorder, such
q 2005 Lippincott Williams & Wilkins

42

Cog Behav Neurol  Volume 18, Number 1, March 2005

Emotional Behavior in Acute Stroke

as impaired sensory input and abnormal representation of body image,42 but the main mechanism is probably a psychodynamic defense mechanism.43 Although denial behavior has been associated with right hemispheric lesions,42 we failed to demonstrate lateralization of the observed denial reaction, possibly because it is too early to distinguish denial behavior during the very acute phase of stroke. In their study, Christensen et al44 found that the score measuring denial reaction gave higher results during the second month post stroke. We could then assume that the development of a full denial disorder occurs only some time after a stroke, which would support the psychologic mechanism rather than organic. Another point of confusion is that anosognosia and denial have been used interchangeably in some studies, although anosognosia refers to the patients inability to recognize his/her own neurologic decit, which is a passive phenomenon, whereas denial refers to an active and delusional refusal to recognize the disease.

Sadness
There have been very few studies on localization of sadness in terms of cerebral mapping. We did not nd any correlation between sadness and a brain region, although an association with bilateral limbic and paralimbic structures has been demonstrated in healthy subjects.45 We found an association of sadness with history of alcohol abuse, which is interesting, as alcohol abuse may be a form of selfmedicating for subclinical affective disorders. That would also allow us to think that premorbid mild mood disorders might play a role in the development of behavior disturbances after stroke.

lesion. Further, more precise anatomicclinical correlation should be undertaken. Cognitive decit and emotional behavior seem to be interrelated, as patients with anosognosia displayed an abnormal behavior more often than patients without anosognosia for almost all categories of the EBI (sadness, passivity, aggressiveness, indifference, and denial), and apraxic and aphasic patients showed more passivity than nonapraxic and nonaphasic patients, respectively. Our ndings support the results of previous studies reporting that anosognosic patients express behavioral correlates of depression, although they deny mood disorders and neurologic decits.50,51 They also support the conclusion of another study52 outlining the role of anosognosia in the diagnosis of poststroke depression, which can be overlooked if diagnostic criteria are based on verbally dependent measurements. In conclusion, the EBI score correlated well with certain cognitive disorders, such as anosognosia, but not with other items, such as physical impairment or lesion properties. Overall, we were unable to conrm several topographic correlations of emotion reported previously. Our study employed a rigorous method based on an observational model but was restricted to a dened period after the stroke and took into consideration only objectively observed emotional behavior. Our work will help in the evaluation of potential early markers of poststroke affective disorders when analyzing patients follow-up after stroke, which is the subject of an ongoing study. Further investigations should also be performed during the acute phase and include other components of emotion, such as vegetative reactions and inner feelings. REFERENCES
1. Kraeplin E. Manic Depressive Insanity and Paranoia. Edinburgh, UK: Livingstone; 1921. 2. Goldstein K. Language and Language Disturbances. New York: Grune and Stratton; 1948. 3. Gainotti G. Emotional behavior and hemispheric side of the lesion. Cortex. 1972;8:4155. 4. Robinson RG, Sarr LB, Lipsey JR, et al. A 2-year longitudinal study of post-stroke mood disorders: dynamic changes in associated variables over the 6 months of follow-up. Stroke. 1984;15:510517. 5. Astrom M, Asplund K, Astrom T. Psychosocial function and life satisfaction after stroke. Stroke. 1992;23:527531. 6. Ahlso B, Britton M, Murray V, et al. Disablement and quality of life after stroke. Stroke. 1964;15:886890. 7. Williams LS, Weinberger M, Harris LE, et al. Development of a strokespecic quality of life scale. Stroke. 1999;30:13621369. 8. Duncan PW, Wallace D, Lai SM, et al. The Stroke Impact Scale version 2.0. Evaluation of reliability, validity, and sensitivity to change. Stroke. 1999;30:21312140. 9. Eysenck HJ. The measurement of emotion: psychological parameters and methods. In: Levi L, ed. Emotions: Their Parameters and Measurements. New York: Raven Press; 1975:439. 10. Toedter LJ, Schall RR, Reese CA, et al. Psychological measures: reliability in the assessment of stroke patients. Arch Phys Med Rehabil. 1995;76:719725. 11. Spence S, Shapiro D, Zaidel E. The role of the right hemisphere in the physiological and cognitive components of emotional processing. Psychophysiology. 1996;33:112122. 12. Meadows ME, Kaplan RF. Dissociation of autonomic and subjective responses to emotional slides in right hemisphere damaged patients. Neuropsychologia. 1994;32:847856. 13. Ghika-Schmid F, Van Melle G, Guex P, et al. Subjective experience and behavior in acute stroke: the Lausanne Emotion in Acute Stroke Study. Neurology. 1999;52:2228.

Emotional Behaviors and Gender

Women seemed to be more expressive than men about sadness and also reported subjective feeling of sadness more often than men. Kring and Gordon46 also reported that women were more emotionally expressive in an experimental study on healthy subjects. This emphasizes the fact that observed emotions may be easier to recognize in women, although we did not see any signicant gender differences in the results for the other categories of the EBI. Women have also been recognized as presenting poststroke depression more often than men in the case of left lesions.47 Indeed, women are also known to be more prone to depression then men also outside the context of cerebral illness.48,49 The exact mechanism, with a probable endocrine component, is still not elucidated.

Emotional Behaviors and Clinical Consequences of Stroke (Motor, Sensory, and Cognitive)
Emotional behavior did not correlate with the degree of physical impairment, supporting the idea that emotions or mood disorders are not just expressions of a reaction to physical impairment but probably have distinct etiologies.32 The fact that we did not identify any correlation between the clinical observation of emotions and the brain lesion should be counterbalanced by the fact that we did consider only large brain subdivisions (anterior/posterior, cortical/subcortical, supra/infratentorial) and did not consider the size of the
q 2005 Lippincott Williams & Wilkins

43

Aybek et al

Cog Behav Neurol  Volume 18, Number 1, March 2005

14. Bogousslavsky J, Van Melle G, Regli F. The Lausanne Stroke Registry: analysis of 1000 consecutive patients with rst stroke. Stroke. 1988;19:10831092. 15. Gainotti G. Disorders of the emotional behavior during cerebral lesions. Schweiz Arch Neurochir Psychiatr. 1976;118:215229. 16. De Agostini M, Blanc-Garin J, de Bonis M. Comptes rendus du Congres ` de Psychiatrie et de Neurologie LXXXIe session. Poitiers, France: Ed Masson; 1983:321328. 17. Berney A, Ghika-Schmid F, Genta F, et al. Comportement emotionnel et accidents vasculaires cerebraux: reliabilite dune echelle de comportement emotionnel. 41eme journees de la Societe de Psychologie Medicale de ` Langue Francaise, Besancon, abstract book; 1998:85. x x 18. Prigatano GP, Schacter DL. Awareness of Decit After Brain Injury. Clinical and Theoretical Issues. New York: Oxford University Press; 1991. 19. Bogousslavsky J. Troubles thymiques et accidents vasculaires cerebraux. Rev Neuropsychologie. 1993;3:257269. 20. Starkstein SE, Fedoroff JP, Price TR, et al. Catastrophic reaction after cerebrovascular lesions: frequency, correlates, and validation of a scale. J Neuropsychiatry Clin Neurosci. 1993;5:189194. 21. House A, Dennis M, Molyneux A, et al. K. Emotionalism after stroke. BMJ. 1989;298:991994. 22. Robinson RG, Parikh RM, Lipsey JR, et al. Pathological laughing and crying following stroke: validation of a measurement scale and a doubleblind treatment study. Am J Psychiatry. 1993;150:286293. 23. Bogousslavsky J, Regli F, Delaloye B, et al. Loss of psychic self-activation with bithalamic infarction. Neurobehavioral, CT, MRI and SPECT correlates. Acta Neurol Scand. 1991;83:309316. 24. Fisher CM. Abulia. In: Bogousslavsky J, Caplyn L, eds. Stroke Syndromes. Cambridge, UK: Cambridge University Press; 1995:182187. 25. Hamilton M. A rating scale for depression. J Neurol Neurosur Psychiatry. 1960;23:5662. 26. Folstein MF, Folstein SE, MacHugh PR. Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189198. 27. Assal G. Batterie des examens neuropsychologiques du CHUV. Lausanne: Division Autonome de Neuropsychologie, 1985. 28. Bisiach E, Vallar G, Perani D, et al. Unawareness of disease following lesions of the right hemisphere: anosognosia for hemiplegia and anosognosia for hemianopia. Neuropsychologia. 1986;24:471482. 29. Tatu L, Moulin T, Bogousslavsky J, et al. Arterial territories of the human brain: brainstem and cerebellum. Neurology. 1996;47:11251135. 30. Tatu L, Moulin T, Bogousslavsky J, et al. Arterial territories of the human brain: cerebral hemispheres. Neurology. 1998;50:16991708. 31. McDowell I, Newell C. Measuring Health: A Guide to Rating Scales and Questionnaires. New York: Oxford University Press; 1996. 32. Fedoroff JP, Starkstein SE, Parikh RM, et al. Are depressive symptoms nonspecic in patients with acute stroke? Am J Psychiatry. 1991; 148:11721176.

33. Robinson RG, Starkstein SE. Current research in affective disorders following stroke. J Neuropsychiatry Clin Neurosci. 1990;2:114. 34. Robinson RG, Kubos KL, Rao K, et al. Mood disorders in stroke patients: importance of location of lesion. Brain. 1984;107:8193. 35. Gainotti G, Azzoni A, Gasparini F, et al. Relation of lesion location to verbal and nonverbal mood measures in stroke patients. Stroke. 1997; 28:21452149. 36. House A, Dennis M, Warlow C. Mood disorders after stroke and their relation to lesion location. A CT scan study. Brain. 1990;113:1113 1129. 37. Singh A, Herrmann N, Black SE. The importance of lesion location in post-stroke depression: a critical review. Can J Psychiatry. 1998;43:921 927. 38. Starkstein SE, Robinson RG. Mechanism of disinhibition after brain lesions. J Nerv Ment Dis. 1997;185:108114. 39. Reeves A, Plum F. Hyperphagia, rage and dementia accompanying a ventromedial hypothalamic neoplasm. Arch Neurol. 1969;20:616624. 40. Haugh RM, Markesbery WR. Hypothalamic astrocytoma: syndrome of hyperphagia, obesity, and disturbances of behavior and endocrine and autonomic function. Arch Neurol. 1983;40:560563. 41. Weiger WA, Bear DM. An approach to the neurology of aggression. J Psychiatr Res. 1988;22:8598. 42. Ellis SJ, Small M. Denial of illness in stroke. Stroke. 1993;24:757759. 43. Weinstein EA, Kahn RL. Denial of Illness: Symbolic and Physiological Aspects. 1955. Springeld, IL: Thomas; 1955. 44. Christensen JM, Cook EA, Martin BC. Identifying denial in stroke patients. Clin Nurs Res. 1997;6:105118. 45. George MS, Ketter TA, Parekh PI, et al. Brain activity during transient sadness and happiness in healthy women. Am J Psychiatry. 1995;152: 341351. 46. Kring AM, Gordon AH. Sex differences in emotion: expression, experience and physiology. J Pers Soc Psychol. 1998;74:686703. 47. Paradiso S, Robinson RG. Gender differences in post-stroke depression. J Neuropsychiatry Clin Neurosci. 1998;10:4147. 48. Arnold LM. Gender differences in bipolar disorder. Psychiatr Clin North Am. 2003;26:595620. 49. Hendricht V, Altshuler LL, Gitlin MJ, et al. Gender and bipolar illness. J Clin Psychiatry. 2000;61:393396. 50. Starkstein SE, Berthier ML, Fedoroff P, et al. Anosognosia and major depression in 2 patients with cerebrovascular lesions. Neurology. 1990;40:13801382. 51. Starkstein SE, Fedoroff JP, Price TR, et al. Anosognosia in patents with cerebrovascular lesions. A study of causative factors. Stroke. 1992; 23:14461453. 52. Ramasubbu R, Kennedy SH. Factors complicating the diagnosis of depression in cerebrovascular disease, part II: neurological decits and various assessment methods. Can J Psychiatry. 1994;39:601607.

44

q 2005 Lippincott Williams & Wilkins