Open Space
Apathy in Acute Stroke and Personality Disturbance Secondary to Stroke
INTRODUCTION
Mental health care and the prevention of mental disease secondary to stroke constitute important areas for research and applied medicine. Stroke itself, and handicaps and dependence after stroke are causes for depression and for loss of motivation or apathy [1].
Apathy appears following uni or bilateral brain lesions involving the caudate, nternal globus pallidus or putamen, or parts of a circuit that includes the medial nucleus of the thalamus and certain frontal regions connected with the limbic system. Lesions or malfunctions in the cortico-subcortical circuit of the anterior cingulate lead to apathy in patients affected by neurological diseases. [2-6]
Recent studies have indicated post-stroke apathy rates of 19-71%, and it was associated with age, low educational levels, right brain lesion, and physical, cognitive and emotional impairments [3, 5, 7-14].
The objective of the present study was to ascertain if apathy in the the acute stage of stroke was a risk factor for Personality Disturbance Secondary to stroke –Apathy Type (Post-stroke apathy), and if post-stroke apathy was related with depression, cognitive impairment, executive and perceptive dysfunctions, or temperament.
METHODS AND PATIENTS
We have systematically evaluated stroke patients (hemorrhagic or ischemic) admitted to the Stroke Unit, Department of Neuroscience, Santa Maria Hospital, up to 7 days following stroke, and re-evaluated at 6 months and 1 year follow-up. All patients gave their informed consent.
Acute evaluation included demographic recordings, and collecting neurological, neuroradiological, neuropsychiatric, and neuropsychological data. Patients with severe communication disturbances based on NIH Stroke Scale [15], and patients with a score of 5-9 in the Glasgow Coma Scale [16] were excluded. They were all subject to a CT or MR scan. Lesions were categorized as: 1) brainstem/cerebellum or hemispheric, 2) hemispheric left or right, 3) hemispheric cortical or subcortical, 4) hemispheric cortical anterior or cortical posterior [17].
The factors deemed to be of risk for apathy were: 1) mild cognitive impairment/dementia (Clinical diagnostic [18] or cognitive subjective complaints) confirmed by a relative; 2) alcohol abuse (=5 drinks per day); 3) previous mood disturbance [18].
At outcome we evaluated the patients’ functional status using the modified Rankin Scale (mRS) [19], post-stroke functional dependence using the Barthel Index [20], and their post-stroke Quality of Life using the EuroQol [21].
The neuropsychiatric and neuropsychological evaluation included apathy assessment using the Apathy Evaluation Scale [1], depression (Montgomery Asberg Depression Rating Scale) [22-23], general cognition (MMSE) [24-25], executive functions (BLAD) [26], emotional perception (Comprehensive Affective Testing System) [27], and temperament (TEMPS) [28].
We used the chi-square to assess bivariate associations between apathy and the remaining variables. We compared the frequencies of neuropsychiatric and neuropsychological disturbances between 2 (McNemar’s test) or 3 (Cochran’s Q test) evaluations (acute and at 6 months and/or 1 year). The Independent T-test and the Paired-Samples T-test were used to compare continuous variables with categorical variables. Pearson’s and Spearman’s tests were used to study the correlations. The value of p=0.05 was statistically significant.
RESULTS
We included 98 patients (61.5±11.4 years old) in the study with a mean of 6.9±4.5 yeas of school,, 67% male, 82% had ischemic lesions, 75% had hemispheric lesions, 49% had right hemispheric lesions and 66% had subcortical lesions. Twenty six patients had a previous mood disorder and eighteen had previous cognitive impairment/mild cognitive impairment.
In acute stage apathy was frequent in 21.4% (21/98) of patients, in 19.4% (14/72) at 6 months, and in 23% (17/76) at 1 year. Apathy in the acute stage was associated with apathy at 6 months (x=5.1; p=.02) and at 1 year (x=3.7; p=.05). At 6 months and 1 year, 40% and 41% of patients suffering from apathy at acute stage remained apathetic, and 57% and 60% new cases of apathy were detected. There was no association between apathy and post-stroke depression, the two coexisting in 8% of patients. No cerebrovascular lesion was associated with post-stroke apathy. Post-stroke apathy was correlated with age and inversely correlated with educational level, functional dependence and quality of life.
Previous mild cognitive impairment/dementia was associated with post-stroke apathy. At 6 months, apathy was associated with emotional perception, and at 1 year it was associated with verbal reasoning disturbances.
Cyclothymic temperament previous to the stroke was associated with apathy at 1 year. No other significant associations were found.
CONCLUSIONS
Post-stroke apathy was frequent in 1/5 of the patients. Apathy at the acute stage of stroke was the strongest indicator of post-stroke apathy, as 40% of patients denoted post-stroke apathy. Age, low educational levels and previous cognitive impairment/dementia were associated with post-stroke apathy. Changes in emotional perception and verbal reasoning were associated with post-stroke apathy. Post-stroke apathy is an indicator of functional dependence and of low quality of life following a stroke..
Lara Caeiro PsyD,
Psychologist, Master Neurosciences,
Institute of Molecular Medicine, Faculty of Medicine, University of Lisbon
laracaeiro@fm.ul.pt
José M. Ferro MD PhD,
Medical Doctor, PhD,
Neurology Service, Department of Neurosciences,
Hospital de Santa Maria, and Faculty of Medicine, University of Lisbon
M. Luísa Figueira MD, PhD
Medical Doctor, PhD,
Psychiatry Service, Department of Neurosciences,
Hospital de Santa Maria, and Faculty of Medicine, University of Lisbon
___________________________
BIBLIOGRAPHIC REFERENCES
1. Marin RS, Biedrzycki RC, Firinciogullari S (1991). Reliability and validity of the apathy evaluation scale. Psychiatry Research 38:143-162.
2. Ghika-Schmid FS e Bogousslavsky J (2000). Emotional behaviours in acute brain lesions In Behaviour and mood disorders in focal brain lesions, Ed. J Bogousslavsky & J L Cummings. Cambridge: University Press; pp: 65-94.
3. Habib M (2000). Disorders of motivation. In: Bogousslavsky J, Cummings JL, editors. Behaviour and mood disorders in focal brain lesions. Cambridge: Cambridge University Press. pp: 261-684.
4. Habib M (1995). Activity and motivational disorders in neurology: proposal for an evaluation scale. Encephale 21:563-70.
5. Bhatia KP and Marsden CD (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain 117: 859-876.
6. Marin RS (1990). Differential diagnosis and classification of apathy. Am J Psychiatry 147:22-30.
7. Santa N, Sugimori H, Kusuda K, Yamashita Y, Ibayashi S, Iida M (2008). Apathy and functional recovery following first-ever stroke.Int J Rehabil Res 31:321-326.
8. Jarzebska E (2007). [Stroke patient’s apathy]. Pol Merkur Lekarski 22: 280-2.
9. Hama S, Yamashita H, Shigenobu M, Watanabe A, Kurisu K, Yamawaki S, Kitaoka T (2007). Post-stroke affective or apathetic depression and lesion location: left frontal lobe and bilateral basal ganglia Eur Arch Psychiatry Clin Neurosci 257:149–152
10. Hama S, Yamashita H, Shigenobu M, Watanabe A, Hiramoto K, Kurisu K, Yamawaki S, Kitaoka T (2007). Depression or apathy and functional recovery after stroke. Int J Geriatr Psychiatry 22:1046-51.9.
11. Brodaty H, Sachdev PS, Withall A, Altendorf A, Valenzuela MJ, Lorentz L (2005). Frequency and clinical, neuropsychological and neuroimaging correlates of apathy following stroke-the Sydney Stroke Study. Psychol Med35:1707-16.
12. Caeiro L (2004). Tese de mestrado. Faculdade de Medicina da Universidade de Lisboa. (Master thesis) Caeiro L, Ferro JM, Figueira ML. Apathy in acute stroke.
13. Hommel M, Trabucco-Miguel S, Joray S, Naegele B, Gonnet N, Jaillard A (2009). Social dysfunctioning after mild to moderate first-ever stroke at vocational age. J Neurol Neurosurg Psychiatry 80:371-5.
14. Feil D, Razani J, Boone K, Lesser I (2003). Apathy and cognitive performance in older adults with depression. Int J Geriatr Psychiatry 18:479-85.
15. Brott T, Adams HP, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V, Rorick M, Moomaw CJ, Walker M (1989). Measurements of acute cerebral infarction: A clinical examination scale. Stroke 20:864-870.
16. Jennett B e Teasdale G (1977). Aspects of coma after severe head injury. The Lancet 23: 878-881.
17. Tatemichi TK, Foulkes MA, Mohr JP, Hewitt JR, Hier DB, Price TR, Wolf PA (1990). Dementia in stroke survivors in the Stroke Data Bank Cohort. Prevalence, incidence, risk factors and computed tomographic findings. Stroke 21:858-66.
18. American Psychiatric Association (APA) (2002). Diagnostic and Statistical Manual of Mental Disorders. 4th Edition, Text Review. DSM IV-TR. American Psychiatric Association: Washington.
19. Bamford JM, Sandercock PAG, Warlow CP, Slattery J (1989). Interobserver agreement for the assessment of handicap in stroke patients. Stroke 20:828.
20. Collin C, Wade DT, Davis S, Horne V (1988). The Barthel index: a reliability study, Int. Disabil. Stud 10: 61–63.
21. Rabin R e De Charro F (2001). EQ-5D: a measure of health status from the Euroqol group, Ann Med 33: 337–343.
22. Caeiro L, Ferro JM, Santos CO, Figueira L (2006). Depression in acute stroke. J Psychiatry Neurosci 31: 377-383.
23. Montgomery S e Asberg M (1979). A new depression rating scale designed to be sensitive to change. Brit J Psychiatry 134: 382-389.
24. Guerreiro M, Botelho MA, Leitão O, Castro-Caldas A, Garcia C (1994). Adaptação à população portuguesa do Mini Mental State Examination (MMSE). Revista Portuguesa de Neurologia: 9-10.
25. Folstein M, Folstein S, Mc Hush P (1975). Mini Mental State, a pratical method for grading the cognitive status of patients for the clinician. J Psychiatr Res 12:189-198.
26. Garcia C (1984). Alzheimer’s disease: difficulties in clinical diagnosis, PhD dissertation, University of Lisbon, Lisbon.
27. Fernandes S (2005). Emotional perception and emotional memory in health subjects. Master thesis presented to the Faculty of Medicine in the Lisbon University.
28. Figueira ML, Caeiro L, Ferro A, Severino L, Duarte PM, Abreu M, Akiskal HS, Akiskal KK (2008). Validation of the Temperament Evaluation of Memphis, Pisa, Paris and San Diego (TEMPS-A): Portuguese-Lisbon version. J. Affect. Disord 111,193-203.
Mental health care and the prevention of mental disease secondary to stroke constitute important areas for research and applied medicine. Stroke itself, and handicaps and dependence after stroke are causes for depression and for loss of motivation or apathy [1].
Apathy appears following uni or bilateral brain lesions involving the caudate, nternal globus pallidus or putamen, or parts of a circuit that includes the medial nucleus of the thalamus and certain frontal regions connected with the limbic system. Lesions or malfunctions in the cortico-subcortical circuit of the anterior cingulate lead to apathy in patients affected by neurological diseases. [2-6]
Recent studies have indicated post-stroke apathy rates of 19-71%, and it was associated with age, low educational levels, right brain lesion, and physical, cognitive and emotional impairments [3, 5, 7-14].
The objective of the present study was to ascertain if apathy in the the acute stage of stroke was a risk factor for Personality Disturbance Secondary to stroke –Apathy Type (Post-stroke apathy), and if post-stroke apathy was related with depression, cognitive impairment, executive and perceptive dysfunctions, or temperament.
METHODS AND PATIENTS
We have systematically evaluated stroke patients (hemorrhagic or ischemic) admitted to the Stroke Unit, Department of Neuroscience, Santa Maria Hospital, up to 7 days following stroke, and re-evaluated at 6 months and 1 year follow-up. All patients gave their informed consent.
Acute evaluation included demographic recordings, and collecting neurological, neuroradiological, neuropsychiatric, and neuropsychological data. Patients with severe communication disturbances based on NIH Stroke Scale [15], and patients with a score of 5-9 in the Glasgow Coma Scale [16] were excluded. They were all subject to a CT or MR scan. Lesions were categorized as: 1) brainstem/cerebellum or hemispheric, 2) hemispheric left or right, 3) hemispheric cortical or subcortical, 4) hemispheric cortical anterior or cortical posterior [17].
The factors deemed to be of risk for apathy were: 1) mild cognitive impairment/dementia (Clinical diagnostic [18] or cognitive subjective complaints) confirmed by a relative; 2) alcohol abuse (=5 drinks per day); 3) previous mood disturbance [18].
At outcome we evaluated the patients’ functional status using the modified Rankin Scale (mRS) [19], post-stroke functional dependence using the Barthel Index [20], and their post-stroke Quality of Life using the EuroQol [21].
The neuropsychiatric and neuropsychological evaluation included apathy assessment using the Apathy Evaluation Scale [1], depression (Montgomery Asberg Depression Rating Scale) [22-23], general cognition (MMSE) [24-25], executive functions (BLAD) [26], emotional perception (Comprehensive Affective Testing System) [27], and temperament (TEMPS) [28].
We used the chi-square to assess bivariate associations between apathy and the remaining variables. We compared the frequencies of neuropsychiatric and neuropsychological disturbances between 2 (McNemar’s test) or 3 (Cochran’s Q test) evaluations (acute and at 6 months and/or 1 year). The Independent T-test and the Paired-Samples T-test were used to compare continuous variables with categorical variables. Pearson’s and Spearman’s tests were used to study the correlations. The value of p=0.05 was statistically significant.
RESULTS
We included 98 patients (61.5±11.4 years old) in the study with a mean of 6.9±4.5 yeas of school,, 67% male, 82% had ischemic lesions, 75% had hemispheric lesions, 49% had right hemispheric lesions and 66% had subcortical lesions. Twenty six patients had a previous mood disorder and eighteen had previous cognitive impairment/mild cognitive impairment.
In acute stage apathy was frequent in 21.4% (21/98) of patients, in 19.4% (14/72) at 6 months, and in 23% (17/76) at 1 year. Apathy in the acute stage was associated with apathy at 6 months (x=5.1; p=.02) and at 1 year (x=3.7; p=.05). At 6 months and 1 year, 40% and 41% of patients suffering from apathy at acute stage remained apathetic, and 57% and 60% new cases of apathy were detected. There was no association between apathy and post-stroke depression, the two coexisting in 8% of patients. No cerebrovascular lesion was associated with post-stroke apathy. Post-stroke apathy was correlated with age and inversely correlated with educational level, functional dependence and quality of life.
Previous mild cognitive impairment/dementia was associated with post-stroke apathy. At 6 months, apathy was associated with emotional perception, and at 1 year it was associated with verbal reasoning disturbances.
Cyclothymic temperament previous to the stroke was associated with apathy at 1 year. No other significant associations were found.
CONCLUSIONS
Post-stroke apathy was frequent in 1/5 of the patients. Apathy at the acute stage of stroke was the strongest indicator of post-stroke apathy, as 40% of patients denoted post-stroke apathy. Age, low educational levels and previous cognitive impairment/dementia were associated with post-stroke apathy. Changes in emotional perception and verbal reasoning were associated with post-stroke apathy. Post-stroke apathy is an indicator of functional dependence and of low quality of life following a stroke..
Lara Caeiro PsyD,
Psychologist, Master Neurosciences,
Institute of Molecular Medicine, Faculty of Medicine, University of Lisbon
laracaeiro@fm.ul.pt
José M. Ferro MD PhD,
Medical Doctor, PhD,
Neurology Service, Department of Neurosciences,
Hospital de Santa Maria, and Faculty of Medicine, University of Lisbon
M. Luísa Figueira MD, PhD
Medical Doctor, PhD,
Psychiatry Service, Department of Neurosciences,
Hospital de Santa Maria, and Faculty of Medicine, University of Lisbon
___________________________
BIBLIOGRAPHIC REFERENCES
1. Marin RS, Biedrzycki RC, Firinciogullari S (1991). Reliability and validity of the apathy evaluation scale. Psychiatry Research 38:143-162.
2. Ghika-Schmid FS e Bogousslavsky J (2000). Emotional behaviours in acute brain lesions In Behaviour and mood disorders in focal brain lesions, Ed. J Bogousslavsky & J L Cummings. Cambridge: University Press; pp: 65-94.
3. Habib M (2000). Disorders of motivation. In: Bogousslavsky J, Cummings JL, editors. Behaviour and mood disorders in focal brain lesions. Cambridge: Cambridge University Press. pp: 261-684.
4. Habib M (1995). Activity and motivational disorders in neurology: proposal for an evaluation scale. Encephale 21:563-70.
5. Bhatia KP and Marsden CD (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain 117: 859-876.
6. Marin RS (1990). Differential diagnosis and classification of apathy. Am J Psychiatry 147:22-30.
7. Santa N, Sugimori H, Kusuda K, Yamashita Y, Ibayashi S, Iida M (2008). Apathy and functional recovery following first-ever stroke.Int J Rehabil Res 31:321-326.
8. Jarzebska E (2007). [Stroke patient’s apathy]. Pol Merkur Lekarski 22: 280-2.
9. Hama S, Yamashita H, Shigenobu M, Watanabe A, Kurisu K, Yamawaki S, Kitaoka T (2007). Post-stroke affective or apathetic depression and lesion location: left frontal lobe and bilateral basal ganglia Eur Arch Psychiatry Clin Neurosci 257:149–152
10. Hama S, Yamashita H, Shigenobu M, Watanabe A, Hiramoto K, Kurisu K, Yamawaki S, Kitaoka T (2007). Depression or apathy and functional recovery after stroke. Int J Geriatr Psychiatry 22:1046-51.9.
11. Brodaty H, Sachdev PS, Withall A, Altendorf A, Valenzuela MJ, Lorentz L (2005). Frequency and clinical, neuropsychological and neuroimaging correlates of apathy following stroke-the Sydney Stroke Study. Psychol Med35:1707-16.
12. Caeiro L (2004). Tese de mestrado. Faculdade de Medicina da Universidade de Lisboa. (Master thesis) Caeiro L, Ferro JM, Figueira ML. Apathy in acute stroke.
13. Hommel M, Trabucco-Miguel S, Joray S, Naegele B, Gonnet N, Jaillard A (2009). Social dysfunctioning after mild to moderate first-ever stroke at vocational age. J Neurol Neurosurg Psychiatry 80:371-5.
14. Feil D, Razani J, Boone K, Lesser I (2003). Apathy and cognitive performance in older adults with depression. Int J Geriatr Psychiatry 18:479-85.
15. Brott T, Adams HP, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V, Rorick M, Moomaw CJ, Walker M (1989). Measurements of acute cerebral infarction: A clinical examination scale. Stroke 20:864-870.
16. Jennett B e Teasdale G (1977). Aspects of coma after severe head injury. The Lancet 23: 878-881.
17. Tatemichi TK, Foulkes MA, Mohr JP, Hewitt JR, Hier DB, Price TR, Wolf PA (1990). Dementia in stroke survivors in the Stroke Data Bank Cohort. Prevalence, incidence, risk factors and computed tomographic findings. Stroke 21:858-66.
18. American Psychiatric Association (APA) (2002). Diagnostic and Statistical Manual of Mental Disorders. 4th Edition, Text Review. DSM IV-TR. American Psychiatric Association: Washington.
19. Bamford JM, Sandercock PAG, Warlow CP, Slattery J (1989). Interobserver agreement for the assessment of handicap in stroke patients. Stroke 20:828.
20. Collin C, Wade DT, Davis S, Horne V (1988). The Barthel index: a reliability study, Int. Disabil. Stud 10: 61–63.
21. Rabin R e De Charro F (2001). EQ-5D: a measure of health status from the Euroqol group, Ann Med 33: 337–343.
22. Caeiro L, Ferro JM, Santos CO, Figueira L (2006). Depression in acute stroke. J Psychiatry Neurosci 31: 377-383.
23. Montgomery S e Asberg M (1979). A new depression rating scale designed to be sensitive to change. Brit J Psychiatry 134: 382-389.
24. Guerreiro M, Botelho MA, Leitão O, Castro-Caldas A, Garcia C (1994). Adaptação à população portuguesa do Mini Mental State Examination (MMSE). Revista Portuguesa de Neurologia: 9-10.
25. Folstein M, Folstein S, Mc Hush P (1975). Mini Mental State, a pratical method for grading the cognitive status of patients for the clinician. J Psychiatr Res 12:189-198.
26. Garcia C (1984). Alzheimer’s disease: difficulties in clinical diagnosis, PhD dissertation, University of Lisbon, Lisbon.
27. Fernandes S (2005). Emotional perception and emotional memory in health subjects. Master thesis presented to the Faculty of Medicine in the Lisbon University.
28. Figueira ML, Caeiro L, Ferro A, Severino L, Duarte PM, Abreu M, Akiskal HS, Akiskal KK (2008). Validation of the Temperament Evaluation of Memphis, Pisa, Paris and San Diego (TEMPS-A): Portuguese-Lisbon version. J. Affect. Disord 111,193-203.
