Aging Medicine and Healthcare 2019;10(4):122-127. doi:10.33879/AMH.2019.122-1811.033 Aging Medicine and Healthcare https://www.agingmedhealthc.com

Original Article Cognitive and Functional Outcomes in Elderly Patients with Post-Stroke Delirium *Efraim Aizen1,2, Igor Yalonnitsky3, Eduard Zalyesov1, Inna Shugaev1

1Fliman Geriatric Rehabilitation Hospital, Haifa, Israel 2Bruce Rappaport Faculty of Medicine, Technion- Institute of Technology, Haifa, Israel 3Department of , Carmel Medical Center, Haifa, Israel

ABSTRACT

Background/Purpose: Delirium is common after stroke in elderly patients and may be associated with short and long-term changes in cognitive function. We aimed to assess disease trajectories and functional outcome in post stroke delirium.

Methods: A prospective study of elderly patients admitted to geriatric rehabilitation after an acute stroke. Patients with delirium were identified with the use of the Confusion Assessment Method (CAM) criteria for delirium. Patients with delirium were assessed daily during hospitalization using the Delirium Rating Scale (DRS-R-98) and the MOTYB test. Functional outcome was assessed in all stroke patients by FIM scores at admission and on discharge and by FIM change and efficiency.

Results: The majority of the 30 participants in whom delirium developed after a stroke continue to be delirious during the hospitalization. Twenty days after admission 19 patients (66.3%) were still delirious. Cognitive performance had *Correspondence a steady improvement until discharge. FIM scores on admission and discharge Dr. Efraim Aizen were significantly lower in stroke patients with delirium. Being a post-stroke Fliman Geriatric delirium patient was independently associated with lower FIM at admission Rehabilitation Hospital, (38.4±9.7 vs. 50.7±18.1; P <0.01), lower FIM at discharge (45.8±14.0 vs. Haifa, Israel 72.5±23.8; P <0.001), lower FIM change (7.5±3.0 vs. 22.9±17.6; P <0.001), and E-mail: lower FIM Efficiency (0.42±0.16 vs. 0.95±0.1; P <0.01). [email protected] The majority of post-stroke delirium patients were still Received 22 November 2018 Conclusion: delirious during the first month of rehabilitation and there was an ongoing Accepted 8 May 2019 improvement in delirium severity until discharge. Post-stroke delirium adversely affects rehabilitation outcome of stroke patients and is associated Keywords with substantial loss of functional independence. Cognitive outcome, delirium, elderly, functional outcome, 2663-8851/Copyright © 2019, Asian Association for Frailty and Sarcopenia and Taiwan storke. Association for Integrated Care. Published by Full Universe Integrated Marketing Limited.

1. INTRODUCTION a high mortality, longer in-patient stay, and higher complication rate, increased risk of institutionalization Delirium is one of the most common complications and increased risk of .1,2 Stroke is a known that elderly patients develop when they are admitted risk factor for the development of delirium.3,4 The to hospital.1 Patients who develop delirium have incidence of delirium in stroke patients varied from

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13% to 48%5 compared to 10% to 25% in patients for inclusion. Patients were excluded if they refused admitted to general internal medicine wards.6 participation, or were severely aphasic; comatose; or were considered too unwell for interview by staff. There have been only a small number of studies that have assessed post-stroke delirium. Usual 2.2. Assessments predisposing conditions are advanced age, an underlying urinary or respiratory infection, and Stroke type (ICH and CI) and location15 was defined preexisting cognitive impairment.4,7 In addition to based on clinical data and on acute computed the usual precipitating factors, the onset of post- tomography/magnetic resonance (CT/MR). If CT/MR stroke delirium is likely to be dependent on several failed to show an acute lesion location was derived factors unique to this clinical setting: the area of brain from clinical data and grouped as: i). brainstem/ affected by the stroke, extent of the stroke, type of cerebellum, hemispherical or both (cortical stroke are stroke, extent of cerebral hypo perfusion and cerebral those affected cortical regions of the cerebral cortex, edema post-stroke, in addition to the development and subcortical strokes affected structures below the of medical complications post-stroke. Specific stroke cortex, including the internal capsule, thalamus, basal types, such as left-sided stroke,8 hemispherical strokes ganglia, brainstem and cerebellum); and ii). left or and intra cerebral hemorrhages,9 cardio embolic right hemispherical or both. Patients were examined stroke and anterior circulation infarction10 may be whenever possible until the second hospitalization more likely to precipitate delirium. In addition, day. The study involved three stages of assessment: delirium may be associated with specific lesions, for Confusion Assessment Method (CAM);16 the Delirium example, in the thalamus and caudate nucleus.11 In Rating Scale (DRS-R-98)17 and formal inattention using essence, large strokes may be more likely to cause MOTYB test (months of the years backwards).18 delirium, but they also are more likely to cause medical complications, which by themselves could CAM is the most widely used screening, which has cause delirium. been validated in several languages and settings.19 We used two kinds of delirium assessment tools that To the best of our knowledge, there is no evidence involved two stages of assessment: Patients who had in the literature about outcomes in acute stroke subjective or objective reports of confusion were patients presenting with delirium. Post-stroke delirium assessed using the sensitive, short form of the CAM, was found to be associated with increased length and deemed either CAM-positive or CAM-negative. of stay, increased in-patient mortality, increased risk We than rated the presence and the severity of the of institutionalization, increased need for geriatric symptoms of delirium according to the DRS-R-98.17 rehabilitation, increased dependence on discharge Patients were diagnosed as having delirium if they and at 6 months, lower MMSE at 6 months and at 12 were CAM-positive and scored ≥10 on DRS-R-98.13 months, and higher 6 and 12 month mortality rate.10-14 Scoring items 2, 3 and 4 of DRS require verbal Patients with post stroke delirium were found to die responses and an awaken patient. Patients with a 4.7-times more likely in the hospital and within 12 moderate or severe communication disturbance months after discharge.14 were excluded from the study. Moderate or severe communication disturbance was defined as a score This study therefore aimed to examine the ≥2 in the Neurological Institute Health Stroke Scale disease trajectories of post stroke delirium after (NIHSS)20 items: severe dysarthria or speech that a rehabilitation-care hospital admission and to cannot be understood and not fully alert patients, determine characteristics, length and factors defined as a GCS score between 5 and 9, scored associated with subsequent resolution of post stroke zero on these items, unless perceptual disturbance, delirium. We also aimed to compare these patient’s hallucinations or delusions were detected by clinical functional outcomes with those who suffered a stroke history or observation. We than rated the presence without developing delirium. and the severity of inattention by the MOTYB test. MOTYB is a simple attention test very useful in 2. METHODS delirium screening. MOTYB used alone is a most accurate screening test in older people.18 For the 2.1. Participants MOTYB, patients were requested to say the months of the year forward from January to December. They Data was prospectively collected over a 6-month were then asked to recite the months in reverse order period (between January 2016 and July 2016) at the from December back to January. Fliman Rehabilitation Geriatric Hospital (an 175-bed public geriatric facility affiliated with the Technion- Pre-existing cognitive decline was considered by University Medical School and located in Haifa, the following pre-stroke predisposing conditions for Israel). All patients over 65 years of age admitted delirium:12 previous medical diagnosis of dementia or consecutively to the five geriatric rehabilitation of mild cognitive impairment or a history of memory wards, with a diagnosis of acute stroke were eligible and another cognitive impairment with functional

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impairment in daily living activities, confirmed by used to characterize the trajectory of delirium scores a proxy. Katz Index of independence in activities over time. We examined the rate of post stroke of daily living (ADL) was used to evaluate the pre- cognitive change over five intervals from baseline (post existing functional ability.21 We utilized the CDR to hospitalization cognitive function): post hospitalization describe the presumed cognitive impairment.22 The day 2, day 3 to 5, 6 to 10, 11 to 15, and 16 to 20 or CDR was obtained through semi structured interviews more. Estimated scores were used for all five intervals of patients and informants, done by well-trained (the estimated score is for the last day of the interval). geriatricians. The CDR utilizes clinical scoring rules In estimating DRS scores, we adjusted for all covariates where CDR 0=no dementia and CDR 0.5, 1, 2, or 3 found statistically different between groups. indicates questionable, mild, moderate, or severe dementia respectively. Baseline information was A second analysis examined recovery over time as gathered during the in-person interview to ascertain measured according to FIM score. We examined function just before the stroke, comorbidity and the functional recovery at two evaluation points aforementioned cognitive screening assessment. (admission and discharge) using all participants Comorbid conditions were obtained from the available at that time period. In estimating delirium participant or proxy respondent and from the medical scores, we adjusted for age, sex, score on the chart using the Charlson Comorbidity Index.23 Charlson Comorbidity Index, and presence or absence of a history of stroke, stroke location and 2.3. Outcomes functional characteristics (previous ADL score and baseline FIM). Overall change within groups was Beginning on hospitalization day 2 and continuing examined by paired samples t-test or Wilcox on until discharge, patients went daily assessment Signed Rank Test, and differences in change between for delirium. Overall, 7% of the daily delirium groups by independent samples t-test or Mann- assessments were missing because of patient or Whitney U Test. staff unavailability (e.g., weekend staffing). The percentage of missing assessments did not differ 3. RESULTS significantly between the patients with and those without delirium. All patients went at least one 3.1. General Characteristics and Description delirium assessment on hospitalization day 2 or 3. The duration of delirium was the first study outcome A total of 110 patients were recruited. The mean (±SD) and was calculated as the number of days between age of the patients was 80.2±8 years, 51.8% women the initial positive delirium assessment and the final (Table 1). The median follow-up time was 42 days. positive delirium assessment. In patients suffering Post-stroke delirium developed in 27.3% of patients from delirium we also monitored the inattention (30 of 110 patients). The mean (±SD) age of these resolution rate by the MOTYB test. patients was 81.5±8.6 years (16 men and 14 women). Eighty controls participated in the study, 37 men and The Functional Independence Measure (FIM) was 43 women aged 79.8±7.8. a second study outcome measure. The FIM is a performance-based disability measure that assesses Of 110 patients recruited, post-stroke delirium level of disability in terms of assistance required to developed in 30 patients (27.3%). As compared perform basic activities of daily living.24,25 It consists of with patients without post-stroke delirium, those 18 items designed to assess the amount of assistance with delirium were more likely to have intra cerebral required to safely perform self-care (6 items), sphincter hemorrhage than cerebral infarcts (Table 1). Patients control (2 items), transfers (3 items), locomotion (2 without post-stroke delirium had similar clinical items), communication (2 items), social adjustment characteristics to the patients with delirium and were and cooperation (3 items), and cognition and problem closely matched for age and sex. solving (3 items). Good reliability and validity have been demonstrated in studies involving orthopedic 3.2. Delirium Severity Score conditions, elderly adults, and individuals with cognitive impairment.24,25 The FIM was completed by Using multilevel modeling, we examined the number trained nurse at admission day and at discharge from of patients diagnosed as suffering from delirium by rehabilitation. the MOTYB score and by the performance on DRS from day 2 onward in post-stroke delirium patients. 2.4. Statistical Analysis After 5 days all delirious patients were still diagnosed by the MOTYB as suffering from delirium. After 10 Baseline characteristics of the stroke patients with and days most patients (28 pts, 93.3%) were still delirious, those without post stroke delirium were compared and after 15 and 20 days the majority of those with the use of the chi-square test for categorical patients were still delirious (21pts, 70% and 19 pts, variables and analysis of variance for continuous 66.3%). The rate of improvement in performance variables. A hierarchical linear regression model was on DRS-R-98 showed a steady drop of 6.4 points on

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Table 1. Baseline characteristics of stroke patients, according to post-stroke delirium status. the DRS-R-98 from baseline until discharge (Table 2). Total Patients Patients with Patients without Characteristics P Value (N=110) Delirium (n=30) Delirium (n=80) Age (yr) 80.2±8.0 81.5±8.6 79.7±7.8 0.32 3.3. Functional Independence Measure (FIM) Scores Gender 0.51 Male (%) 53 (48.2) 16 (53.3) 37 (46.3) Admission total FIM scores were Female (%) 57 (51.8) 14 (46.7) 43 (53.8) significantly lower in the post- stroke delirium group (37.5±9.7 vs. History of previous stroke (%) 28 (25.5) 8 (26.7) 20 (25.0) 0.86 50.8±19.3); (P <0.001); additionally, Charlson Comorbidity Index 4.3±1.9 4.4±1.8 4.2±2.0 0.71 post-stroke delirium patients were Cognitive status (CDR) 0.35±0.60 0.38±0.52 0.34±0.62 0.76 discharged with significantly lower Stroke type <0.001 total FIM scores (45.4±14.7 vs. 72.8±26.1) (P <0.001), compared CI (%) 87 (79.1) 16 (53.3) 71 (88.8) with patients without delirium ICH (%) 23 (20.9) 14 (46.7) 9 (11.2) (Table 3). Additionally, FIM scores Stroke location 0.46 change and efficiency were significantly lower in the post- Cortical (%) 56 (50.9) 17 (56.7) 39 (48.8) stroke delirium group (7.2±11.4 Sub-cortical (%) 54 (49.1) 13 (43.3) 41 (51.3) vs. 22.1±17.6 and 0.39±0.75 vs. Stroke side 0.53 0.96±0.88), respectively); (P <0.001 P Right (%) 49 (44.6) 16 (53.3) 33 (41.3) and <0.01, respectively). Left (%) 48 (43.6) 11 (36.7) 37 (46.2) We carried out a one-way Bilateral (%) 13 (11.8) 3 (10.0) 10 (12.5) ANCOVA test to determine a Previous ADL score 4.88±1.47 4.67±1.58 4.91±1.46 0.46 statistically significant difference between delirious patients and patients without delirium on FIM scores, whilst Table 2. Estimates of DRS test over time. controlling for demographic, functional and clinical Estimated Daily Change characteristics. This showed that being a post-stroke Estimated Score† (95% CI) delirium patient was independently associated with Day 2 20.7±2.9 poorer total FIM scores at admission (38.4±9.7 vs. Day 3-5 18.8±3.5 -1.9 (-3.0 to -0.7) 50.7±18.1; P <0.01) (Table 4). Being a post-stroke delirium patient was also independently associated Day 6-10 17.1±2.95 -1.2 (-3.2 to -0.4) with poorer total FIM scores at discharge (45.8±14.0 Day 11-15 15.6±3.2 -1.4 (-1.4 to -0.2) vs. 72.5±23.8; P <0.001). Additionally, being a post- Day 16-20 14.3±3.3 -1.3 (-2.3 to -0.3) stroke delirium patient was independently associated †The estimated score is for the last day of the interval. with poorer FIM scores change and efficiency (7.5±3.0 vs. 22.9±17.6 and 0.42±0.16 vs. 0.95±0.1, respectively); (P <0.001 and P <0.01, respectively). Table 3. Functional recovery over time of stroke patients, according to post-stroke delirium status (unadjusted association). 4. DISCUSSION Functional Patients with Patients without P Value Variable Delirium (n=30) Delirium (n=80) We found that the majority of post-stroke delirium FIM at admission 37.5±9.7 50.8±19.3 <0.001 patients are still delirious during the first month of FIM at discharge 45.4±14.7 72.8±26.1 <0.001 rehabilitation after the stroke (66.3% after 20 days). FIM change 7.2±11.4 22.0±17.6 <0.001 The rate of improvement in performance on DRS FIM efficiency 0.39±0.75 0.96±0.88 <0.01 showed a prolonged steady improvement from baseline until discharge.

Table 4. Functional recovery over time of stroke patients, according The rate of delirium resolution is dependent on the to post-stroke delirium status (adjusted for demographic and methods used for its ascertainment, and our study clinical characteristics). used a rigorous assessment with diagnosis by means Functional Patients with Patients without of the CAM and the DRS-R-98, the most widely P Value Variable Delirium (n=30) Delirium (n=80) adopted, validated approach in the literature. The FIM at admission 38.4±9.7 50.7±18.1 <0.01 MOTYB test is a very good individual screening test for delirium, with a sensitivity of 83.3% and FIM at discharge 45.8±14.0 72.5±23.8 <0.001 a specificity of 90.8%18 Our results imply that the FIM change 7.5±3.0 22.9±17.6 <0.001 MOTYB as a formal attention testing is useful FIM efficiency 0.42±0.16 0.95±0.10 <0.01 in delirium screening but may be less accurate

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in tracking complete resolution of the delirium regression analysis, accounting for the effect of syndrome in these patients. However, since attention different demographic and clinical confounders, and and concentration are important functioning during support our assumption that functional rehabilitation rehabilitation, our finding that after 20 days on outcomes of adults with delirium after stroke are rehabilitation, attention in these patients did not inferior in comparison to patients who suffered stroke improve beyond the threshold of delirium screening without developing delirium afterwards. ability in 66.3% of the patients, may be important in regards to the cognitive rehabilitation. Such results, showing that patients who experienced delirium in the acute stage of stroke were more The second tool we used was the DRS-R-98, a valid likely to have unfavorable outcomes by means and reliable symptom severity scale for delirium.17 of standardized assessment of ability to perform It is a validated delirium rating instrument with activities of daily living were published before.9,10,13,26,29 sufficient breadth and detail for use in longitudinal But to the best of our knowledge, this is the first study studies of delirium patients. We assessed cognitive to compare the effects of post stroke delirium on on average of five times during the rehabilitation rehabilitation outcomes using the more accurate FIM period, allowing us to accurately model the course of which was have demonstrated good reliability and cognitive function. Using the DRS-R-98, we found that validity in rehabilitation.24,25 delirium after stroke was associated with a post stroke cognitive trajectory characterized by a prolonged Other studies that have addressed outcomes of post period of impairment. These findings suggest that stroke delirium, showed that suffering from delirium delirium might have longer-term observed effects after a stroke is a negative predictor for successful on cognitive function in patients who have suffered functional recovery. These finding are not surprising, a stroke. We did not find other studies that have considering the fact that patients suffering from addressed the effect of delirium on the course of delirium after a stroke are generally described as more cognitive function after stroke. vulnerable, having higher baseline morbidity and even mortality rates.4,8-10,30 The marked functional loss in our Our findings are of clinical significance, since study is alarming, considering the fact that patients we found that patients with post stroke delirium with delirium were not found to have higher incidence continued to have improvement throughout the of cognitive impairment before suffering the stroke. rehabilitation period. Given that delirium is associated with poor functional recovery after stroke4,10,12,26 and The present study is advantageous in the sense that cognitive impairment is associated with poor that it is a prospective study that comprised a big functional recovery after hospital discharge,27,28 our enough sample of patients, all of whom suffered finding has implications for the duration of post a stroke and underwent a rehabilitation program stroke care and rehabilitation services after suffering in a ward dedicated to the rehabilitation of elderly a stroke. Since patients with post stroke delirium may stroke patients. Another advantage is the use of continue to have improvements in cognitive function the FIM as a structured assessment tool. The use after discharge from rehabilitation, and rehabilitation of FIM to analyze our data is advantageous, as it services may need to be extended for these patients. shows lower ceiling and floor effects compared with other scales. This probably helps with measuring Since the risk of delirium among patients suffering a with greater accuracy the functional gains during stroke is very high, multi factorial prevention methods rehabilitation. Nevertheless, certain limitations should should be well tested in these patients. Findings such be considered: first, the study cohort was restricted as ours argue for further development and testing to elderly hospitalized for rehabilitation a few days of interventions designed for better evaluation and after a stroke. Assessing only this cohort, disregards treatment of delirium after stroke. In patients with post patients who suffered a stroke and developed a short stroke delirium, cognitive screening at rehabilitation period delirium that resolved before rehabilitation admission may identify high-risk patients who require admission. Second, although the study sample close monitoring in order to enhance functional and was not big, this study provides helpful preliminary clinical outcomes. data for recovery of function in the rehabilitation setting. Third, although the natural history of delirium The present prospective study also focused on trajectory was described, mediators of improvement the relationship between delirium after stroke and cannot be commented on. For example, it is unknown rehabilitation outcome as assessed by the FIM whether rehabilitation therapy or expertise was similar score. Results of the univariate analysis suggested in both groups, although in our hospital, such patients that delirium after stroke is associated with worse usually receive the same rehabilitation program. FIM scores on admission and discharge and poorer functional gains (FIM scores change and Several additional factors that we were unable to efficiency) during rehabilitation. These results examine may have contributed to our findings. remained statistically significant after using multiple Factors such as polypharmacy, malnutrition, sensory

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impairment, depression or medical complications 12. Gustafson Y, Olsson T, Asplund K, Hägg E. Acute confusional might influence recovery from delirium. state (delirium) soon after stroke is associated with Hypercortisolism. Cerebrovasc Dis. 1993;3:33-8. 5. CONCLUSION 13. Henon H, Lebert F, Durieu I, Godefroy O, Lucas C, Pasquier F, et al. Confusional state in stroke. Relation to preexisting dementia, patient characteristics and outcome. Stroke. 1999;30:773-9. This prospective study of elderly patients suffering a stroke and delirium showed that the rate of 14. Shi Q, Presutti R, Selchen D, Saposnik G. Delirium in acute stroke: a systematic review and meta-analysis. Stroke. improvement of the delirium symptoms severity 2012;43:645-9. was a prolonged steady improvement from baseline 15. Tatemichi TK, Foulkes MA, Mohr JP, Hewitt JR, Hier DB, Price until discharge. Another important point revealed in TR, et al. Dementia in stroke survivors in the Stroke Data Bank this study is that elderly patients, who suffered from Cohort. Prevalence, incidence, risk factors and computed delirium after being hospitalized for in rehabilitation tomographic findings. Stroke. 1990;21:858-66. after a stroke, had little recovery of functional status 16. Inouye SK, van Dyck CH, Alessi CA, Balkin S, Siegal AP, Horwitz compared with adults who suffered stroke without RI. Clarifying confusion: the confusion assessment method. delirium. Identifying patients at high risk for delirium A new method for detection of delirium. Ann Intern Med. and promoting the development of interventions to 1990;113:941-8. prevent delirium in patients after stroke may reduce 17. Trzepacz PT. The Delirium Rating Scale. Its use in consultation- the rate of long-term cognitive impairment in this liaison research. Psychosomatics. 1999;40:193-204. population. Patients in whom delirium develops 18. O'Regan NA, Ryan DJ, Boland E, Connolly W, McGlade C, after a stroke may require further interventions and Leonard M, et al. Attention! A good bedside test for delirium? J Neurol Neurosurg Psychiatry. 2014; :1122-31. customized rehabilitation programs to optimize 85 recovery. 19. Ely EW, Margolin R, Francis J, May L, Truman B, Dittus R, et al. Evaluation of delirium in critically ill patients: validation of the Confusion Assessment Method for the Intensive Care Unit CONFLICTS OF INTEREST (CAM-ICU). Crit Care Med. 2001;29:1370-9.

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