Emotional Disturbances after Stroke

Abstract

Impairment after stroke may have acute and long-lasting psychological implications. Additionally, organic brain dysfunction also appears to play an important role in poststroke affective modifications. Emotional state is multidetermined and can be specifically modified by alteration of some brain networks. This article illustrates a certain number of acute and more chronic emotional disturbances after stroke, such as mood disorders, emotional dyscontrol, and modification of emotional experiences. Some neural mechanisms implicated in these modifications are discussed. The main modifications described are depression anxiety, psychosis, modification of emotional experience, and fatigue.

Full text

Clinical and Experimental Hypertension, 28:243–249, 2006
Copyright © Taylor & Francis Group, LLC
ISSN: 1064-1963 print / 1525-6006 online
DOI: 10.1080/10641960600549173
243
LCEH1064-19631525-6006Clinical and Experimental Hypertension, Vol. 28, No. 03, February 2006: pp. 0–0Clinical and Experimental Hypertension
Emotional Disturbances after Stroke
Emotional DisturbancesJ.-M. Annoni et al. JEAN-MARIE ANNONI,1,2 FABIENNE STAUB,1
LAURE BRUGGIMANN,1 SANDRINE GRAMIGNA,1 AND
JULIEN BOGOUSSLAVSKY1
1Department of Neurology, University Hospital, Lausanne, Switzerland
2Department of Neurology, University Hospital, Geneva, Switzerland
Impairment after stroke may have acute and long-lasting psychological implications.
Additionally, organic brain dysfunction also appears to play an important role in
poststroke affective modifications. Emotional state is multidetermined and can be
specifically modified by alteration of some brain networks. This article illustrates a
certain number of acute and more chronic emotional disturbances after stroke, such as
mood disorders, emotional dyscontrol, and modification of emotional experiences.
Some neural mechanisms implicated in these modifications are discussed. The main
modifications described are depression anxiety, psychosis, modification of emotional
experience, and fatigue.
Introduction
From the neurological point, emotion is a multicomponential process in response to exter-
nal and internal stimuli, which implicates perceptive (fear, joy, disgust), motivational
(arousal), autonomic (sympathetic reaction), motor response, and cognitive evaluation (1).
Emotional changes can affect short-lasting processing like emotional reaction or long-
standing states like mood. After stroke, emotional disturbances include mood disorders,
emotional dyscontrol, and alteration of emotional reactions. They are of utmost impor-
tance and certainly unrecognized by clinicians, not only in the acute phase, but also in the
chronic stage, when behavioral changes are noted. It has been recognized that emotional
state is not only an important part of the feeling of well-being but also it has high influence
on patients’ behavior. Behavior, which refers to the manner in which a person acts in a
given situation, is influenced by a multitude of cognitive and emotional lexicons, like
information from our semantic memory—including moral knowledge—our pattern of
preferences, our emotional states, and our pattern of reactivity (impulsivity or apathy).
A simple example of a classic emotional disturbance in the acute phase of stroke is
the anosognosia for the disease, that although exemplified in the Anton-Babinski
syndrome, reflects a typical tendency of the brain to neglect perceptual loss (2). Such
tendency partly explains why stroke patients take much longer time to arrive at the
Address correspondence to Jean-Marie Annoni, MD, Department of Neurology, University
Hospital, CH-1011 Lausanne, Switzerland; E-mail: Jean-marie.annoni@chuv.hospvd.ch
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244 J.-M. Annoni et al.
emergency department, while it takes less than 2 hr for a cardiac infarct. Another mecha-
nism that can explain defective cognitive-emotional integration is what can be called
“acute memory or acute remembering impairment” in patients with acute stroke (3).
According to these, up to 33% of stroke patients have no, or only a poor, memory of
what actually happened during the acute phase. The interesting aspect is that this usually
occurs without specific damage to the classic anatomical structures known to be involved
in learning. Whether this is an acute phenomenon, perhaps linked to some kind of “sider-
ation” of brain function or to the natural brain difficulty to recognize a neurological
impairment, is not always clear. We often call this anosognosia, although this term lumps
together quite different conditions, that can include the patient being convinced that he or
she is not ill, does not have motor impairment, does not have a potentially severe medical
condition, or does not have a brain problem. The particularity of these impairments during
acute phase can explain why immediate poststroke emotional changes are different from
the more chronic stages.
Acute Stage
One problem in looking at the literature is that descriptions combine the acute and chronic
consequences of stroke. For instance, mania and mania-like states may really be acute
phase problems, as is catastrophic reaction, seen in some patients very early in the course
of stroke, whereas depression, by definition, is a chronic manifestation. One of the main
issues is that in contrast to the plethora of studies on poststroke depression several weeks,
months, or years after stroke, emotion and behavior during the acute stroke phase have
received very little attention.
At Lausanne, we have developed the Emotional Behavioural Index, that can be com-
pleted by nurses in continuous care units. Its advantage is that it provides a description,
rather than an interpretation, of behavior in acute stroke patients (4). In principle, depres-
sion already is a diagnosis, i.e., it is already an interpretation of the facts rather than a
simple description that the patient looks sad or is crying. The measurement of behavior
may be much closer to reality, especially in patients with communications problems, e.g.,
aphasics, who are usually systematically excluded from studies because of their communi-
cation problems. The Emotional Behavioural Index bypasses the need for language
communication (5).
In our experience in over 300 acute patients, overt sadness is the most common
manifestation (72%), followed by disinhibition (56%), lack of adaptation (44%), envi-
ronmental withdrawal (40%), crying (27%), anosognosia (24%), passivity (24%), and
aggressiveness (11%). Overt sadness is more frequently associated with left (86%) rather
than right (61%) hemisphere lesions (p < 0.05), and the association is even greater in
the case of crying (50% versus 20% for left and right hemisphere lesions, respectively;
p= 0.02). With right-side lesions, anosognosia is clearly associated with neglect (95%
versus 34% for neglect versus nonneglect, respectively; p = 0.01). However, with right
hemisphere lesions, both sadness and indifference also are more frequent in anosognosic
patients. It is interesting to see that even in right hemisphere stroke, sadness is not absent
by any means.
Moreover, anosognosia may coexist with severe sadness, that at first sight may seem
paradoxical. However, it is obvious that sadness, even leading to depression in some
cases, actually can develop in patients who are not really aware of their own condition (6).
A particular emotional modification in the acute phase is the catastrophic reaction (CR) in
acute stroke (7). The prevalence is as low as 3% (n = 12 among 326 patients with
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Emotional Disturbances 245
first-ever stroke), but the very strong correlation with the presence of aphasia (100%
patients were aphasics) and with left insular location suggests that it is an emotional
behavior that is induced by specific network damage. It also has been interpreted as
“reflex” or “avoidance” behavior more than a psychological reaction. Interestingly, 66%
of patients with CR developed depression in the chronic stage.
Acute phase emotional changes also can present psychosis. Acute psychosis has been
described rarely but in a precise way after acute stroke. In the case of Low, an 82-year-old
man was admitted very restless, agitated, and noisy and was shouting and screaming
incessantly, after a left posterior cerebral artery infarct (8).
Chronic Phase
Depression
Poststroke depression (PSD) is not rare, occurring in ∼40% of stroke victims, with minor
and major poststroke depression occurring in equal proportions. Data from different studies
have found prevalence rates for major depression of 19.3% among hospitalized patients
and 23.3% among outpatient samples (9). Although in our group the proportion of PSD
patients remains similar at 12 months than at 3 months (∼35% in both groups), the late
depression are different patients than the early depressed (10).
The cause of PSD has been associated with left anterior lesion location in numerous
independent studies. Although a meta-analysis (11) of PSD and lesion location failed to
find a significant association, it seems that during the first 2 months after an acute stroke,
left frontal and left basal ganglia lesions were significantly more frequent among patients
with major depression compared with any other lesion location (9).
Furthermore, another meta-analysis of the literature examining the correlation
between severity of depression and proximity of the lesion to the left frontal pole found a
significant correlation (pooled correlation coefficient: r = −.53 fixed model, r = −.59
random model) for patients who were less than 6 months poststroke (12). Interestingly,
some findings suggest that left stroke could be a predictor of treatment resistance to selec-
tive serotonin reuptake inhibitors (13). These results fit with the ones obtained in control
subjects on the role of left frontal areas on positive thinking.
The chronic PSD and anxiety also are more frequent in patients with subcortical
(white matter, thalamus, basal ganglia) or brain stem lesion. One recent finding in biolog-
ical psychiatry is the fact that silent brain infarcts and cerebral white matter lesions on
magnetic resonance imaging (MRI) were found to be more frequent in the depressed
elderly than in controls. Cerebral small vessel disease has been rediscovered as a potential
cause of depression (14).
Clinically, this shows important differences from what psychiatrists call endogenous
depression. Even severe cases of PSD are not identical to endogenous depression, as they
have much more reactive diurnal mood variation and emotionalism, show an absence of
guilt, and are rarely suicidal. Among 142 patients with 2-year follow-up, the psychologi-
cal symptoms that were not significantly more frequent in the depressed compared with
the nondepressed group were suicide plans, simple ideas of reference, pathologic guilt
irritability, and self-depreciation (15). Gainotti (16) comparing patients with poststroke
major depression with 30 patients found that patients with endogenous depression (i.e., no
associated brain injury) had higher scores on anhedonia and suicide, and patients with
PSD had higher scores on hyperemotionalism, catastrophic reactions, and diurnal mood
variation.
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246 J.-M. Annoni et al.
Anxiety Disorders
Anxiety disorders are frequent (∼ 25%) after strokes (17). Furthermore, heavy cognitive def-
icits increase difficulty in recognizing anxiety, supporting the need for more studies in minor
strokes. In a prospective study including 90 patients assessed 6 months after a minor stroke,
isolated significant anxious scores were present in 26/90 patients (29%) Hospital Anxiety
and Depression Scale, anxiety > or = to 8). In particular, symptoms consistent with posttrau-
matic stress disorder (PTSD) can occur after stroke as a consequence of the sudden occur-
rence of a life-threatening event. One year after stroke, posttraumatic-like symptoms were
present in 15 of the 49 patients (31%) who completed the impact event scale (IES; > or = to
30). PTSD-like syndrome was independent of neurological impairment, physical disability,
and nosognosia during hospitalization and peristroke amnesia, but it was more frequent in
patients who felt concerned about death in the acute phase. Concerning lesion localization,
no specific lesion localization was associated with PTSD symptoms. Nevertheless, intrusive
symptoms were increased after lesions involving basal ganglia strokes, suggesting that re-
experiencing phenomena may be modulated by frontal-subcortical pathways (18, 19).
Mania and Bipolar Disorders
Mania seems to be related more strongly to right hemispheric lesions. One study found
that of 9 patients with mania following stroke, 8 had right hemisphere lesions, while in
major depression in which only 7 of 31 patients had right hemisphere strokes (20). While
major depression during the acute stroke period was associated with left frontal and left
basal ganglia lesions, mania was associated with right orbital frontal, basotemporal, basal
ganglia (21), or thalamic lesions (22). In addition, when poststroke patients with mania
were compared with poststroke patients matched for lesion size and location, the mania
patients had significantly greater subcortical atrophy (23–25).
Psychosis
Psychosis is quite rare after stroke. Among 157 patients following their first stroke, the
frequency of all depressive disorders was 17.2%, but no cases of mania or psychosis were
found (26). Some other clinical pictures take the form of “delusional misidentification
syndromes” (DMS), that include “reduplicative paramnesia” (RP) for places, reduplica-
tion of people, events, objects, and roles; Capgras’ syndrome where an impostor is thought
by the patient replaces the real person, and numerous variations such as Fregoli syndrome,
intermetamorphosis syndrome, the “reverse” syndromes.
Some observations suggest that DMS is a functional disconnection between past mne-
sic information and the ability to integrate them with actual experiences (28). Although
most of the DMS are related to diffuse brain dysfunction, some can be induced by stroke.
Some isolated case reports suggest that left perilimbic lesions may play a role in the devel-
opment of psychotic symptoms (29, 30). Susceptibility to develop schizophreniform ill-
ness after stroke includes pre-existing subcortical, atrophy, and right hemisphere lesion
location of the stroke (31).
Emotional Hyperactivity and Flattening
Mood swing and emotional hyperactivity are well known after bilateral cerebrovascular
lesion and in vascular dementia. Some of them are associated with emotional disinhibition
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Emotional Disturbances 247
with outburst and loss of emotional control, as in basal ganglia and frontal degenerative
pathologies (32, 33).
Emotional flattening is the frequent consequence of amygdala or medioventral frontal
cortex damage (34) and can be associated with impaired autonomic reactivity. However,
blunting of affect or disinhibited and inappropriate behaviors can be observed—together
with executive and other cognitive dysfunction—in patients with lesions involving the
posterior lobe of the cerebellum and the vermis (35). This type of emotional flattening
seems to be associated with an impaired autonomic system response to the emotional
valence of stimuli (36).
Poststroke Fatigue
In our study, we have defined fatigue as a reversible decrease or loss of abilities associated with
a heightened sensation of physical or mental strain, even without conspicuous effort. This con-
dition is due to an overwhelming feeling of exhaustion, that leads to an inability to sustain, or a
difficulty in sustaining, even routine activities. Preliminary data show that patients with fatigue
can be depressed, but that a large cohort (20% to 50%) of patients are not (37). The important
aspect is that patients with poststroke fatigue do not show either severe neurological distur-
bance or functional impairment. Our preliminary findings emphasize that patients with so-
called primary poststroke fatigue may have mainly brain stem lesions (38). At 1 year, there was
a significant association of fatigue with young age, neurological impairment, and anxiety lev-
els (for cortical and subcortical lesions), and with attentional performances for cortical lesions.
There was no significant association with laboratory workup (cortisol, thyroxine, Thyrotropin
Releasing Hormone, adeno-corticotropic hormone).
We speculate that many cases of poststroke fatigue may correspond to subtle attentional
dysfunction, although neuropsychological assessment shows no cognitive-executive distur-
bance. Some researchers noted that the patients with a postpolio fatigue syndrome had spe-
cific neuropsychological disorders with attentional difficulties and slowing of information
processing speed. A cognitive profile was compatible with an impairment of basal ganglia
and reticular activating system. The neuroanatomical studies (autopsic Magnetic Resonance
Imaging and studies) indeed revealed constant and severe lesions in the reticular formation,
hypothalamic and thalamic nuclei, and basal ganglia, thus showing that the poliovirus dam-
ages cerebral areas responsible for cortical activation. Finally, the authors found a significant
negative correlation between fatigue and level of plasmatic adrenocorticotropic hormone
suggesting a hypofunctionning of the hypothalamic-pituitary-adrenal axis (39).
Acknowledgments
This work was supported by the Swiss National Science Foundation grant number
3151AO-102271 to J.-M. Annoni and 3200–061342.00 to J. Bogousslavsky. We thank
Cephalon very much for his contribution in the present study. A short study about the
effect of modafinil on fatigue after stroke is in progress.
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