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Prevalence, Course, and Risk Factors for Executive Impairment in Patients Hospitalized on a General Medicine Service
Prevalence, Course, and Risk Factors for Executive Impairment in Patients Hospitalized on a General Medicine Service JASON E. SCHILLERSTROM, M.D., MONICA S. HORTON, M.D. TRACY L. SCHILLERSTROM, M.D., KAUSTUBH G. JOSHI, M.D. BRIAN S. EARTHMAN, M.D., ANGELA M. VELEZ, M.D. DONALD R. ROYALL, M.D.
The purpose of this study was to determine the prevalence, course, and risk factors for executive impairment in patients hospitalized on a general medicine service. One hundred patients were administered the Executive Interview (EXIT25), the Executive Clock Drawing Task (CLOX), and the Mini-Mental State Examination at admission and discharge. Fifty-two percent of the patients at admission and 56% at discharge had scores indicating impairment on at least one measure of executive function. Median scores on every measure improved during hospitalization. Older patients and those with a cardiac or gastrointestinal disorder were more likely to have executive impairment. The prevalence of executive impairment on general medicine services is high. Although improvement in executive function occurs during hospitalization, many patients remained impaired. (Psychosomatics 2005; 46:411–417)
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xecutive function is the ability to plan, initiate, sequence, monitor, and inhibit complex behavior.1 Emerging data suggest the presence of executive impairment in patients with medical disorders such as cancer, chronic obstructive pulmonary disease, diabetes, HIV, hypertension, and systemic lupus erythematosus.2–7 In one study, 72% of medicine and surgery patients seen by a psychiatry consultation service had scores indicating impairment on at least one measure of executive function.8 The failure to identify medically ill patients with executive impairments could have important clinical consequences, especially with regard to medication adherence, preservation of autonomy, relapse prevention, postdischarge placement, and potential for rehabilitation. The purpose of the study reported here was to determine the prevalence and course of executive impairment in patients hospitalized on a general medicine service and to identify potential risk factors for executive impairment in this population. Psychosomatics 46:5, September-October 2005
METHOD Subjects Institutional review board approval for this study was obtained from the University of Texas Health Science Center at San Antonio. Patients were consecutively recruited from three general medicine services during a 6-week period at a public teaching hospital. At this hospital, patients with neurological disease such as stroke are cared for by a separate neurology service and thus were not recruited. Any English- or Spanish-speaking patient age 18 years or Received Jan. 29, 2004; revision received May 13, 2004; accepted June 15, 2004. From the Departments of Psychiatry, Medicine, and Pharmacology, University of Texas Health Science Center at San Antonio. Address correspondence and reprint requests to Dr. Schillerstrom, Department of Psychiatry, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78229; schillerstr@ uthscsa.edu (e-mail). Copyright 䉷 2005 The Academy of Psychosomatic Medicine.
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Executive Impairment older was eligible for inclusion. Exclusion criteria included mental retardation and pregnancy. Patients who were prisoners and patients who could not physically participate in testing, such as those with motor deficits, were also excluded. Because we wanted to identify executive impairment in the absence of delirium, patients transferred from other services such as the surgical service or the intensive care unit were excluded, as were those who screened positive for delirium according to the Confusion Assessment Method.9 The comparison group consisted of spouses and siblings of hospitalized patients. Each patient was evaluated by one of six physicians who collected data and administered the cognitive tests. No investigator was a member of any patient’s treatment team. Medical care and diagnostic formulation were provided by clinicians who were blinded to the psychometric measures. Comparison subjects self-reported their medical and psychiatric diagnoses and medications. Cognitive Tests The Executive Interview (EXIT25), the Executive Clock Drawing Task (CLOX), and the Mini-Mental State Examination (MMSE) were administered. Each patient was tested within 24 hours after admission and before discharge, and therefore patients who were hospitalized less than 2 days generally were tested only once. Comparison subjects were tested only once during the course of their relative’s hospitalization. EXIT25 The EXIT25 is a 25-item multitask assessment of executive function that is easily administered at the bedside.10 Scores on the EXIT25 correlate strongly with scores on other executive measures including the Wisconsin Card Sorting Test (r⳱0.54), Lezak’s Tinker Toy Test (r⳱0.57), Test of Sustained Attention (time, r⳱0.82; errors, r⳱ 0.83), and Trail Making Part B (r⳱0.64).10 The interrater reliability of the EXIT 25 is high (r⳱0.90).10 An EXIT25 score of ⱖ15 of 50 indicates executive impairment. This score best discriminated well elderly retirees from those in supervised settings and best predicted capacity to give informed consent for health care.10,11 This cutoff score was equally valid in young adults with schizophrenia.12 However, it may underestimate the prevalence of executive impairment in younger patients, because one study showed that a score of 10 of 50 best discriminates between young adult patients with and without HIV-associated dementia.13 412
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CLOX The CLOX is composed of two components.14 For CLOX 1, the patient is asked to draw a clock after being given the following instructions: “Draw a clock that says 1:45. Set the hands and numbers on the face so that a child could read them.” The clock is scored on a scale of 1 to 15. A score ⱕ10 of 15 for CLOX1 represents the lowest 5th percentile for young adults.14 CLOX1 scores correlate significantly, but moderately, with EXIT25 scores, suggesting that the two instruments may detect different dimensions of executive function.15 CLOX1 is more sensitive to executive impairment, as measured by the EXIT25, than are similar clock-drawing tasks.16 Scores on both the EXIT25 and CLOX1 make significant independent contributions to variance in Wisconsin Card Sorting Test scores and disability in older adults.15,17 CLOX2 is a measure of simple constructional praxis that assesses drawing ability, tremor, and vision. During CLOX2, the examiner draws a clock for the patient and then asks the patient to copy it. The scoring system used for CLOX1 is also used for CLOX2. A CLOX2 scoreⱕ12 of 15 represents the lowest 5th percentile for young adults.14 CLOX2 scores correlate strongly with MMSE scores (r⳱0.85).14 Interrater reliability (CLOX 1: r⳱0.94, CLOX 2: r⳱0.93; both p⬍0.001) and internal consistency (Cronbach alpha⳱0.82) are high for both tasks.14 Both the EXIT25 and the CLOX are available in Spanish language translations, and the CLOX has been validated for use with Hispanic people.18 MMSE The MMSE is perhaps the most commonly used instrument for evaluation of general cognitive impairment.19 However, it does not assess executive impairment, and patients who have an MMSE score within normal limits may have scores indicating impairment on executive measures.20 Although cutoff scores for this instrument are controversial, we used a conventional cutoff score of ⱕ24 to indicate impairment.21 Data Analysis The statistical software used for data analysis was NCSS/PASS 2000 Dawson Edition (NCSS, Kaysville, Utah). All alpha levels were set to 0.05. The prevalence of executive impairment was determined by calculating the percentage of patients with scores on the EXIT25 or CLOX1 in the ranges designated by the listed cutoff points. Chi-square analysis was used to search for significant differences between the percentage of patients and compariPsychosomatics 46:5, September-October 2005
Schillerstrom et al. son subjects with scores in these ranges. The Wilcoxon rank sum test was used to compare test score medians between the two groups. The course of cognitive impairment in hospitalized patients was assessed by using the Wilcoxon rank sum test to compare the median admission and discharge test scores for patients with 2 or more days of hospitalization. McNemar’s test was used to determine if a significant number of patients changed from having scores indicating impairment on the cognitive measures at admission to having scores within the normal limits at discharge. Potential risk factors for executive impairment included age, education, number of morbidities (including the presenting morbidity and any comorbidities), number of medications (both scheduled and as-needed medications), and number of days hospitalized. Two-tailed t tests were used to compare the mean value of these variables between patients with scores above and below the cutoff point for the EXIT25. Chi-square analysis was used to search for significant gender and ethnicity differences between those with scores above and below the cutoff point for the EXIT25. To determine if patients in certain diagnostic categories were more prone to cognitive impairment, the patients were grouped by their admitting diagnosis. A diagnostic category had to have a minimum of six patients to be included in the analysis; diagnostic categories with less than six patients were grouped together in the “other” category. A total of seven categories were created: endocrine disorders, gastrointestinal disorder, cardiac disorder, cancer, infection, pulmonary disorder, and “other.” The median admission EXIT25 and CLOX1 scores of the patients in each diagnostic category were compared with those of the comparison group. RESULTS Subjects’ Characteristics A total of 224 patient contacts were made during a 6week period, and 100 patients enrolled in the study. Fortyfive refused, 68 were excluded, and 11 were missed within the 24-hour time period for data collection. Of the 100 patients enrolled in the study, 60 had a 2-day or longer length of hospitalization; discharge testing was performed with 38 of those patients (63.3%). The 22 patients who did not complete discharge testing either refused, were discharged against medical advice, were discharged before the evaluation by the research team, or were transferred to anPsychosomatics 46:5, September-October 2005
other service. The average length of hospitalization for all patients in the study was 3.77 days. Fifty nonhospitalized comparison subjects consented to participate and enrolled. Table 1 shows the demographic characteristics of the hospitalized patient group and the nonhospitalized comparison group. Admission and Discharge Cognitive Test Scores EXIT25 The median score of the patients at admission was significantly greater than the median score of the comparison group (Table 2). Forty-two percent (N⳱42) of the patients scored below the cutoff point for impairment on the EXIT25 at admission, compared with 18% (N⳱9) of the comparison subjects (v2⳱8.56, df⳱1, p⬍0.01). There was no significant difference between the patients’ median admission and median discharge scores (Table 3). There was no significant difference between the number of patients with an EXIT25 score above the cutoff for impairment at admission and the number with a score in that range at discharge. CLOX1 There was no significant difference between the median score of the patients at admission and the median score of the comparison group. Twenty-five percent (N⳱25) of the patients had a score below the cutoff point for impairment at admission, compared to 20% (N⳱10) of the comparison subjects (v2⳱0.51, df⳱1, p⬎0.05). The median CLOX1 score of the patients was significantly higher at discharge, compared to admission (Table 3). There was a significant difference between the number of patients with a CLOX1 score below the cutoff point for impairment at admission and the number at discharge (McNemar’s test⳱4.5, df⳱1, p⬍0.05). Fifty-two percent of the patients had a score indicating impairment on either the EXIT25 or the CLOX1 at admission, compared to 32% of the comparison group (v2⳱5.92, df⳱1, p⬍0.05). Of the 38 patients who were hospitalized for more than 48 hours, 17 had a score indicating impairment on at least one executive measure at admission, compared to 11 patients at discharge (McNemar’s test⳱4.5, df⳱1, p⬍0.05). CLOX2 There was no significant difference between the median score of the patients at admission and the median score of the comparison group. Fifteen percent of the patients scored below the cutoff point for impairment on the CLOX2 at admission, compared to 16% of the comparison group (v2⳱0.006, df⳱1, p⬎0.05). There was no signifihttp://psy.psychiatryonline.org
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Executive Impairment cant difference between the patients’ median admission score and median discharge score. There was no significant difference between the number of patients with a score below the cutoff point for impairment at admission and the number with a score in that range at discharge. MMSE The median admission MMSE score for patients was significantly lower than that for the comparison group (Table 2). Nine percent of the patients scored below the cutoff point for impairment on the MMSE at admission, compared to 4% of the comparison group (v2⳱1.23, df⳱1, p⬎0.05). There was no significant difference between the patients’ median admission score and median discharge score. There was no significant difference between the number of patients with an MMSE score within the normal limits at admission and the number with a score in that range at discharge.
ber of medications, and number of days hospitalized were not significantly different between the patients with an EXIT25 score above the cutoff point for impairment and those with a score below the cutoff point in any diagnostic group. Patients with a cardiac or gastrointestinal disorder had median admission EXIT25 scores that were significantly higher than those of the comparison group (Table 4). No differences were found between the median admission CLOX1 score of patients in any diagnostic category and that of the comparison group. Patients with a cardiac disorder were significantly older than the comparison subjects (mean⳱58.7 years, SD⳱11.5, versus mean⳱46.5 years, SD⳱14.4; T⳱2.14, df⳱53, p⳱0.04). Sixteen patients had a documented psychiatric disorder as a secondary diagnosis. Of these patients, only two had EXIT25 scores indicating impairment. No patient or comparison subject had a diagnosis of dementia.
Risk Factors for Executive Impairment DISCUSSION Patients with EXIT25 scores within the normal limits were significantly younger than those with scores above the cutoff for impairment in every group tested—the entire study group (mean⳱44.1 years, SD⳱12.3, versus mean⳱52.8 years, SD⳱14.8; T⳱3.26, df⳱98, p⳱0.002), patients hospitalized for 2 days or more tested at admission (mean⳱42.3 years, SD⳱12.6, versus mean⳱53.3 years, SD⳱13.5; T⳱3.26, df⳱58, p⳱0.002), and patients hospitalized for 2 days or more who were tested at discharge (mean⳱44.6 years, SD⳱13.3, versus mean⳱55.9 years, SD⳱13.8; T⳱2.27, df⳱36, p⳱0.03). Gender distribution, ethnicity distribution, mean educational level, number of morbidities, numTABLE 1.
This pilot study is marked by several limitations. The first limitation is the small number of subjects. Although 100 subjects is a large enough group for estimation of the prevalence of executive impairment on a general medicine service, this group size does not allow detection of anything less than strong risk factors for executive impairment. In addition, illnesses were categorized on the basis of the systems involved, which is imprecise. Important diagnostic categories, such as renal disorders, hematological disorders, and substance withdrawal, were collapsed into the “other” category for analysis. Despite this limitation, our findings may provide direction for future studies. Previous
Demographic Characteristics of Patients Hospitalized on a General Medicine Service and Nonhospitalized Comparison Subjects in a Study of Executive Impairment Nonhospitalized Comparison Subjects (Nⴔ50)
Hospitalized Patients (Nⴔ100) Characteristic a
Male Ethnic group Hispanic Caucasian African American Other Age (years) Educationb
N
%
N
%
50
50
14
28
61 26 11 2 Mean 47.8 10.9
61 26 11 2 SD 14.0 3.5
30 10 8 1 Mean 46.5 11.7
60 20 16 2 SD 14.4 3.0
Significant difference between groups (v2⳱6.16, df⳱1, p⬍0.05). Highest grade level completed.
a
b
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Schillerstrom et al. authors have found executive impairment in patients with heart disease,22 but little is known about the association between gastrointestinal disorder and executive impairment. Finally, the patients and comparison subjects were not screened for depression, which is also associated with executive deficits. The data for the comparison subjects are also limited. We depended on the comparison subjects’ self-report of medical illness and medications. Only two comparison subjects had MMSE scores below the cutoff indicating impairment, suggesting that the self-reports in this group might be accurate.23 However, the MMSE is a poor preTABLE 2.
dictor of other forensic capacities, such as the capacity to give informed consent.24 In contrast, EXIT25 scores are strongly associated with a variety of forensic capacities, including the capacity to make an advance directive and the capacity to give informed consent for medical care.11,25,26 Eighteen percent of the comparison subjects had EXIT25 scores indicating impairment, although persons similar to the comparison subjects—siblings and spouses of hospitalized patients—are frequently asked to provide substituted consent or ancillary history for incapacitated patients on medical inpatient wards. We report on the prevalence of executive impairment
Admission Cognitive Test Scores of Patients Hospitalized on a General Medicine Service and Nonhospitalized Comparison Subjectsa Nonhospitalized Comparison Subjects
Hospitalized Patients Test Executive Interview (EXIT25) Executive Clock Drawing Task (CLOX) CLOX1 CLOX2 Mini-Mental State Examination
Analysis
N
Median
95% CI
N
Median
95% CI
z
p
100
13
11–15
50
9.5
8–12
ⳮ2.32
0.02
99 99 100
12 13 28
12–12 13–14 28–28
50 50 50
11–13 13–14 29–30
0.75 1.01 2.60
12 14 29
0.45 0.31 0.009
a Patients were tested within 24 hours of admission; nonhospitalized comparison subjects, who were siblings and spouses of the patients, were tested during the course of the patients’ hospitalization.
TABLE 3.
Cognitive Test Scores at Admission and Discharge of Patients Hospitalized for ⱖ2 Days on a General Medicine Service Admission
Discharge
Analysis
Test
N
Median
95% CI
N
Median
95% CI
z
p
Executive Interview (EXIT25) Executive Clock Drawing Task (CLOX) CLOX1 CLOX2 Mini-Mental State Examination
60
11
9–16
38
11
6–14
ⳮ1.56
0.11
59 59 60
12 13 28
11–12 13–14 27–29
38 38 38
13 14 29
12–14 13–14 28–29
3.94 1.70 1.20
TABLE 4.
⬍0.001 0.09 0.23
Admission Executive Interview (EXIT25) Scores of Patients in Various Diagnostic Categories Hospitalized on a General Medicine Service and Nonhospitalized Comparison Subjects Analysisa
EXIT25 Score Group and Diagnostic Category
N
Median
95% CI
z
p
Hospitalized patients Cancer Cardiac disorder Endocrine disorder Gastrointestinal disorder Infection Pulmonary disorder Other Nonhospitalized comparison subjects
10 7 6 15 31 14 17 50
14.5 17 16 14 12 10 11 9.5
4–28 9–25 6–20 9–21 7–16 6–14 8–16 8–12
1.50 2.01 1.73 2.60 1.31 0.29 1.02 —
0.13 0.04 0.08 0.01 0.19 0.78 0.31 —
a
For comparison of hospitalized patients and nonhospitalized comparison subjects.
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Executive Impairment as measured by the EXIT25 and CLOX1. Although 52% of the patients scored in the range indicating impairment on one or the other of these measures, these measures may not represent a comprehensive assessment of executive function, which has multiple dimensions.27 We observed a high degree of overlap in the patients identified as executively impaired by these measures, and it is possible that the addition of other measures of executive function might have further increased the prevalence of executive impairment, relative to the prevalence we report. However, such findings would only strengthen our conclusion that executive impairment is common among medical inpatients. Executive impairment may improve through the course of usual standard-of-care medical management, but further study of this outcome is needed. Fifty-six percent of the patients in our study were discharged back to the community after having scored in the range indicating impairment on at least one measure of executive function within the previous 24 hours. This high rate of executive impairment probably was not detected by clinicians, as only 4% of the patients scored below the MMSE cutoff score for impairment within 24 hours of discharge. Furthermore, some patients may be discharged with worse ex-
ecutive function than they had at admission, as evidenced by our finding that 5% of the patients with an EXIT25 score indicating impairment at discharge had a score within the normal limits at admission. We conclude that as many as one-half of medical inpatients are vulnerable to executive impairment. The MMSE is insensitive to this impairment and should not be used as the sole cognitive screening test in this setting. Executive impairment may undermine the quality of information obtained from patients, undermine attempts to obtain informed consent for treatment, undermine treatment adherence, and complicate efforts to discharge patients safely. Moreover, a significant fraction of the caregivers available to assist in these matters may have similar impairments. Further study is warranted to confirm our findings and further explore medical risk factors for executive impairment. This project was funded in part by an unrestricted educational grant from the Department of Psychiatry of the University of Texas Health Science Center at San Antonio. The first author received the American Psychiatric Association/Lilly Resident Research Award for this body of work.
References
1. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders, 4th Edition, Text Revision. Washington, DC, American Psychiatric Association, 2000, pp 147–171 2. Komaki R, Meyers CA, Shin DM, Garden AS, Byrne K, Nickens JA, Cox JD: Evaluation of cognitive function in patients with limited small cell lung cancer prior to and shortly following prophylactic cranial irradiation. Int J Radiat Oncol Biol Phys 1995; 33:179–182 3. Grant I, Heaton RK, McSweeny AJ, Adams KM, Timms RM: Neuropsychologic findings in hypoxemic chronic obstructive pulmonary disease. Arch Intern Med 1982; 142:1470–1476 4. Lowe LP, Tranel D, Wallace RB, Welty TK: Type II diabetes and cognitive function: a population-based study of Native Americans. Diabetes Care 1994; 17:891–896 5. Stern Y, Liu X, Marder K, Todak G, Sano M, Ehrhardt A, Gorman J: Neuropsychological changes in a prospectively followed cohort of homosexual and bisexual men with and without HIV infection. Neurol 1995; 45:467–472 6. Sahakian BJ, Elliot R, Low N, Mehta M, Clark RT, Pozniak AL: Neuropsychological deficits in tests of executive function in asymptomatic and symptomatic HIV-1 seropositive men. Psychol Med 1995; 25:1233–1246 7. Blumenthal JA, Madden DJ, Pierce TW, Siegel WC, Appelbaum M: Hypertension affects neurobehavioral functioning. Psychosom Med 1993; 55:44–50 8. Schillerstrom JE, Deuter MS, Wyatt R, Stern SL, Royall DR: Prevalence of executive impairment in patients seen by a psychiatry consult service. Psychosomatics 2003; 44:290–297 9. Inouye SK, van Dyck CH, Alessi CA, Balkin S, Siegal AP, Hor-
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witz RI: Clarifying the confusion: the confusion assessment method. Ann Intern Med 1990; 113:941–948 10. Royall DR, Mahurin RK, Gray KF: Bedside assessment of executive cognitive impairment: the executive interview. J Am Geriatr Soc 1992; 40:1221–1226 11. Holzer JC, Gansler DA, Moczynski NP, Folstein M: Cognitive functions in the informed consent evaluation process. J Am Acad Psychiatry Law 1997; 25:531–540 12. Royall DR, Mahurin RK, True J, Anderson B, Brock IP 3rd, Freeburger L, Miller A: Executive impairment among the functionally dependent: comparison between schizophrenic and elderly subjects. Am J Psychiatry 1993; 150:1813–1819 13. Berghuis JP, Uldall KK, Lalonde B: Validity of two scales in identifying HIV-associated dementia. J Acquir Immune Defic Syndr Hum Retrovirol 1999; 21:134–140 14. Royall DR, Cordes JA, Polk M: CLOX: an executive clock drawing task. J Neurol Neurosurg Psychiatry 1998; 64:588–594 15. Royall DR, Chiodo LK, Polk MJ: Correlates of disability among elderly retirees with “sublclinical” cognitive impairment. J Gerontol A Biol Sci Med Sci 2000; 55A:M541–546 16. Royall DR, Mulroy AR, Chiodo LK, Polk MJ: Clock drawing is sensitive to executive control: a comparison of six methods. J Gerontol A Biol Sci Med Sci 1999; 54:328–333 17. Royall DR, Chiodo LK, Polk MJ: Bedside measures as proxies for Wisconsin Card Sort performance in old age. J Neuropsychiatry Clin Neurosci 1997; 9:684–685 18. Royall DR, Espino DV, Polk MJ, Verdeja R, Vale S, Gonzales H, Palmer RR, Markides KP: Validation of Spanish translation of the CLOX for use in Hispanic samples: the hispanic epese study. Int J Geriatr Psychiatry 2003; 18:135–141
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Schillerstrom et al. 19. Folstein M, Folstein S, McHugh PR: ‘Mini mental state’: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189–198 20. Nebes RD, Reynolds CF 3rd, Boada F, Meltzer CC, Fukui MB, Saxton J, Halligan EM, DeKosky ST: Longitudinal increase in the volume of white matter hyperintensities in late-onset depression. Int J Geriatr Psychiatry 2002; 17:526–530 21. Kaplan HI, Sadock BJ (eds): Delirium, dementia, and amnestic and other cognitive disorders and mental disorders due to a general medical condition, in Synopsis of Psychiatry: Behavioral Sciences/Clinical Psychiatry, 8th ed. Baltimore, Williams & Wilkins, 1998, pp 318–364 22. Moser DJ, Cohen RA, Clark MM, Aloia MS, Tate BA, Stefanik S, Forman DE, Tilkemeier PL: Neuropsychological functioning among cardiac rehabilitation patients. J Cardiopulmonary Rehabilitation 1999; 19:91–97 23. Edelberg HK, Shallenberger E, Wei JY: Medication management
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capacity in highly functioning community-living older adults: detection of early deficits. J Am Geriatr Soc 1999; 47:592–596 24. Etchells E, Katz MR, Shuchman M, Wong G, Workman S, Choudhry NK, Craven J, Singer PA: Accuracy of clinical impressions and mini-mental state exam scores for assessing capacity to consent to major medical treatment. Psychosomatics 1997; 38:239–259 25. Royall DR, Cordes J, Polk M: Executive control and the comprehension of medical information by elderly retirees. Exp Aging Res 1997; 23:301–313 26. Dymek MP, Atchison P, Harrell L, Marson DC: Competency to consent to medical treatment in cognitively impaired patients with Parkinson’s disease. Neurology 2001; 56:17–24 27. Royall DR, Lauterbach EC, Cummings JL, Reeve A, Rummans TA, Kaufer DI, LaFrance WC Jr, Coffey CE: Executive control function: a review of its promise and challenges for clinical research: a report from the Committee on Research of the American Neuropsychiatric Association. J Neuropsych Clin Neurosci 2002; 14:377–405
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The purpose of this study was to determine the prevalence, course, and risk factors for executive impairment in patients hospitalized on a general medicine service. One hundred patients were administered the Executive Interview (EXIT25), the Executive Clock Drawing Task (CLOX), and the Mini-Mental State Examination at admission and discharge. Fifty-two percent of the patients at admission and 56% at discharge had scores indicating impairment on at least one measure of executive function. Median scores on every measure improved during hospitalization. Older patients and those with a cardiac or gastrointestinal disorder were more likely to have executive impairment. The prevalence of executive impairment on general medicine services is high. Although improvement in executive function occurs during hospitalization, many patients remained impaired. (Psychosomatics 2005; 46:411–417)
E
xecutive function is the ability to plan, initiate, sequence, monitor, and inhibit complex behavior.1 Emerging data suggest the presence of executive impairment in patients with medical disorders such as cancer, chronic obstructive pulmonary disease, diabetes, HIV, hypertension, and systemic lupus erythematosus.2–7 In one study, 72% of medicine and surgery patients seen by a psychiatry consultation service had scores indicating impairment on at least one measure of executive function.8 The failure to identify medically ill patients with executive impairments could have important clinical consequences, especially with regard to medication adherence, preservation of autonomy, relapse prevention, postdischarge placement, and potential for rehabilitation. The purpose of the study reported here was to determine the prevalence and course of executive impairment in patients hospitalized on a general medicine service and to identify potential risk factors for executive impairment in this population. Psychosomatics 46:5, September-October 2005
METHOD Subjects Institutional review board approval for this study was obtained from the University of Texas Health Science Center at San Antonio. Patients were consecutively recruited from three general medicine services during a 6-week period at a public teaching hospital. At this hospital, patients with neurological disease such as stroke are cared for by a separate neurology service and thus were not recruited. Any English- or Spanish-speaking patient age 18 years or Received Jan. 29, 2004; revision received May 13, 2004; accepted June 15, 2004. From the Departments of Psychiatry, Medicine, and Pharmacology, University of Texas Health Science Center at San Antonio. Address correspondence and reprint requests to Dr. Schillerstrom, Department of Psychiatry, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78229; schillerstr@ uthscsa.edu (e-mail). Copyright 䉷 2005 The Academy of Psychosomatic Medicine.
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Executive Impairment older was eligible for inclusion. Exclusion criteria included mental retardation and pregnancy. Patients who were prisoners and patients who could not physically participate in testing, such as those with motor deficits, were also excluded. Because we wanted to identify executive impairment in the absence of delirium, patients transferred from other services such as the surgical service or the intensive care unit were excluded, as were those who screened positive for delirium according to the Confusion Assessment Method.9 The comparison group consisted of spouses and siblings of hospitalized patients. Each patient was evaluated by one of six physicians who collected data and administered the cognitive tests. No investigator was a member of any patient’s treatment team. Medical care and diagnostic formulation were provided by clinicians who were blinded to the psychometric measures. Comparison subjects self-reported their medical and psychiatric diagnoses and medications. Cognitive Tests The Executive Interview (EXIT25), the Executive Clock Drawing Task (CLOX), and the Mini-Mental State Examination (MMSE) were administered. Each patient was tested within 24 hours after admission and before discharge, and therefore patients who were hospitalized less than 2 days generally were tested only once. Comparison subjects were tested only once during the course of their relative’s hospitalization. EXIT25 The EXIT25 is a 25-item multitask assessment of executive function that is easily administered at the bedside.10 Scores on the EXIT25 correlate strongly with scores on other executive measures including the Wisconsin Card Sorting Test (r⳱0.54), Lezak’s Tinker Toy Test (r⳱0.57), Test of Sustained Attention (time, r⳱0.82; errors, r⳱ 0.83), and Trail Making Part B (r⳱0.64).10 The interrater reliability of the EXIT 25 is high (r⳱0.90).10 An EXIT25 score of ⱖ15 of 50 indicates executive impairment. This score best discriminated well elderly retirees from those in supervised settings and best predicted capacity to give informed consent for health care.10,11 This cutoff score was equally valid in young adults with schizophrenia.12 However, it may underestimate the prevalence of executive impairment in younger patients, because one study showed that a score of 10 of 50 best discriminates between young adult patients with and without HIV-associated dementia.13 412
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CLOX The CLOX is composed of two components.14 For CLOX 1, the patient is asked to draw a clock after being given the following instructions: “Draw a clock that says 1:45. Set the hands and numbers on the face so that a child could read them.” The clock is scored on a scale of 1 to 15. A score ⱕ10 of 15 for CLOX1 represents the lowest 5th percentile for young adults.14 CLOX1 scores correlate significantly, but moderately, with EXIT25 scores, suggesting that the two instruments may detect different dimensions of executive function.15 CLOX1 is more sensitive to executive impairment, as measured by the EXIT25, than are similar clock-drawing tasks.16 Scores on both the EXIT25 and CLOX1 make significant independent contributions to variance in Wisconsin Card Sorting Test scores and disability in older adults.15,17 CLOX2 is a measure of simple constructional praxis that assesses drawing ability, tremor, and vision. During CLOX2, the examiner draws a clock for the patient and then asks the patient to copy it. The scoring system used for CLOX1 is also used for CLOX2. A CLOX2 scoreⱕ12 of 15 represents the lowest 5th percentile for young adults.14 CLOX2 scores correlate strongly with MMSE scores (r⳱0.85).14 Interrater reliability (CLOX 1: r⳱0.94, CLOX 2: r⳱0.93; both p⬍0.001) and internal consistency (Cronbach alpha⳱0.82) are high for both tasks.14 Both the EXIT25 and the CLOX are available in Spanish language translations, and the CLOX has been validated for use with Hispanic people.18 MMSE The MMSE is perhaps the most commonly used instrument for evaluation of general cognitive impairment.19 However, it does not assess executive impairment, and patients who have an MMSE score within normal limits may have scores indicating impairment on executive measures.20 Although cutoff scores for this instrument are controversial, we used a conventional cutoff score of ⱕ24 to indicate impairment.21 Data Analysis The statistical software used for data analysis was NCSS/PASS 2000 Dawson Edition (NCSS, Kaysville, Utah). All alpha levels were set to 0.05. The prevalence of executive impairment was determined by calculating the percentage of patients with scores on the EXIT25 or CLOX1 in the ranges designated by the listed cutoff points. Chi-square analysis was used to search for significant differences between the percentage of patients and compariPsychosomatics 46:5, September-October 2005
Schillerstrom et al. son subjects with scores in these ranges. The Wilcoxon rank sum test was used to compare test score medians between the two groups. The course of cognitive impairment in hospitalized patients was assessed by using the Wilcoxon rank sum test to compare the median admission and discharge test scores for patients with 2 or more days of hospitalization. McNemar’s test was used to determine if a significant number of patients changed from having scores indicating impairment on the cognitive measures at admission to having scores within the normal limits at discharge. Potential risk factors for executive impairment included age, education, number of morbidities (including the presenting morbidity and any comorbidities), number of medications (both scheduled and as-needed medications), and number of days hospitalized. Two-tailed t tests were used to compare the mean value of these variables between patients with scores above and below the cutoff point for the EXIT25. Chi-square analysis was used to search for significant gender and ethnicity differences between those with scores above and below the cutoff point for the EXIT25. To determine if patients in certain diagnostic categories were more prone to cognitive impairment, the patients were grouped by their admitting diagnosis. A diagnostic category had to have a minimum of six patients to be included in the analysis; diagnostic categories with less than six patients were grouped together in the “other” category. A total of seven categories were created: endocrine disorders, gastrointestinal disorder, cardiac disorder, cancer, infection, pulmonary disorder, and “other.” The median admission EXIT25 and CLOX1 scores of the patients in each diagnostic category were compared with those of the comparison group. RESULTS Subjects’ Characteristics A total of 224 patient contacts were made during a 6week period, and 100 patients enrolled in the study. Fortyfive refused, 68 were excluded, and 11 were missed within the 24-hour time period for data collection. Of the 100 patients enrolled in the study, 60 had a 2-day or longer length of hospitalization; discharge testing was performed with 38 of those patients (63.3%). The 22 patients who did not complete discharge testing either refused, were discharged against medical advice, were discharged before the evaluation by the research team, or were transferred to anPsychosomatics 46:5, September-October 2005
other service. The average length of hospitalization for all patients in the study was 3.77 days. Fifty nonhospitalized comparison subjects consented to participate and enrolled. Table 1 shows the demographic characteristics of the hospitalized patient group and the nonhospitalized comparison group. Admission and Discharge Cognitive Test Scores EXIT25 The median score of the patients at admission was significantly greater than the median score of the comparison group (Table 2). Forty-two percent (N⳱42) of the patients scored below the cutoff point for impairment on the EXIT25 at admission, compared with 18% (N⳱9) of the comparison subjects (v2⳱8.56, df⳱1, p⬍0.01). There was no significant difference between the patients’ median admission and median discharge scores (Table 3). There was no significant difference between the number of patients with an EXIT25 score above the cutoff for impairment at admission and the number with a score in that range at discharge. CLOX1 There was no significant difference between the median score of the patients at admission and the median score of the comparison group. Twenty-five percent (N⳱25) of the patients had a score below the cutoff point for impairment at admission, compared to 20% (N⳱10) of the comparison subjects (v2⳱0.51, df⳱1, p⬎0.05). The median CLOX1 score of the patients was significantly higher at discharge, compared to admission (Table 3). There was a significant difference between the number of patients with a CLOX1 score below the cutoff point for impairment at admission and the number at discharge (McNemar’s test⳱4.5, df⳱1, p⬍0.05). Fifty-two percent of the patients had a score indicating impairment on either the EXIT25 or the CLOX1 at admission, compared to 32% of the comparison group (v2⳱5.92, df⳱1, p⬍0.05). Of the 38 patients who were hospitalized for more than 48 hours, 17 had a score indicating impairment on at least one executive measure at admission, compared to 11 patients at discharge (McNemar’s test⳱4.5, df⳱1, p⬍0.05). CLOX2 There was no significant difference between the median score of the patients at admission and the median score of the comparison group. Fifteen percent of the patients scored below the cutoff point for impairment on the CLOX2 at admission, compared to 16% of the comparison group (v2⳱0.006, df⳱1, p⬎0.05). There was no signifihttp://psy.psychiatryonline.org
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Executive Impairment cant difference between the patients’ median admission score and median discharge score. There was no significant difference between the number of patients with a score below the cutoff point for impairment at admission and the number with a score in that range at discharge. MMSE The median admission MMSE score for patients was significantly lower than that for the comparison group (Table 2). Nine percent of the patients scored below the cutoff point for impairment on the MMSE at admission, compared to 4% of the comparison group (v2⳱1.23, df⳱1, p⬎0.05). There was no significant difference between the patients’ median admission score and median discharge score. There was no significant difference between the number of patients with an MMSE score within the normal limits at admission and the number with a score in that range at discharge.
ber of medications, and number of days hospitalized were not significantly different between the patients with an EXIT25 score above the cutoff point for impairment and those with a score below the cutoff point in any diagnostic group. Patients with a cardiac or gastrointestinal disorder had median admission EXIT25 scores that were significantly higher than those of the comparison group (Table 4). No differences were found between the median admission CLOX1 score of patients in any diagnostic category and that of the comparison group. Patients with a cardiac disorder were significantly older than the comparison subjects (mean⳱58.7 years, SD⳱11.5, versus mean⳱46.5 years, SD⳱14.4; T⳱2.14, df⳱53, p⳱0.04). Sixteen patients had a documented psychiatric disorder as a secondary diagnosis. Of these patients, only two had EXIT25 scores indicating impairment. No patient or comparison subject had a diagnosis of dementia.
Risk Factors for Executive Impairment DISCUSSION Patients with EXIT25 scores within the normal limits were significantly younger than those with scores above the cutoff for impairment in every group tested—the entire study group (mean⳱44.1 years, SD⳱12.3, versus mean⳱52.8 years, SD⳱14.8; T⳱3.26, df⳱98, p⳱0.002), patients hospitalized for 2 days or more tested at admission (mean⳱42.3 years, SD⳱12.6, versus mean⳱53.3 years, SD⳱13.5; T⳱3.26, df⳱58, p⳱0.002), and patients hospitalized for 2 days or more who were tested at discharge (mean⳱44.6 years, SD⳱13.3, versus mean⳱55.9 years, SD⳱13.8; T⳱2.27, df⳱36, p⳱0.03). Gender distribution, ethnicity distribution, mean educational level, number of morbidities, numTABLE 1.
This pilot study is marked by several limitations. The first limitation is the small number of subjects. Although 100 subjects is a large enough group for estimation of the prevalence of executive impairment on a general medicine service, this group size does not allow detection of anything less than strong risk factors for executive impairment. In addition, illnesses were categorized on the basis of the systems involved, which is imprecise. Important diagnostic categories, such as renal disorders, hematological disorders, and substance withdrawal, were collapsed into the “other” category for analysis. Despite this limitation, our findings may provide direction for future studies. Previous
Demographic Characteristics of Patients Hospitalized on a General Medicine Service and Nonhospitalized Comparison Subjects in a Study of Executive Impairment Nonhospitalized Comparison Subjects (Nⴔ50)
Hospitalized Patients (Nⴔ100) Characteristic a
Male Ethnic group Hispanic Caucasian African American Other Age (years) Educationb
N
%
N
%
50
50
14
28
61 26 11 2 Mean 47.8 10.9
61 26 11 2 SD 14.0 3.5
30 10 8 1 Mean 46.5 11.7
60 20 16 2 SD 14.4 3.0
Significant difference between groups (v2⳱6.16, df⳱1, p⬍0.05). Highest grade level completed.
a
b
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Schillerstrom et al. authors have found executive impairment in patients with heart disease,22 but little is known about the association between gastrointestinal disorder and executive impairment. Finally, the patients and comparison subjects were not screened for depression, which is also associated with executive deficits. The data for the comparison subjects are also limited. We depended on the comparison subjects’ self-report of medical illness and medications. Only two comparison subjects had MMSE scores below the cutoff indicating impairment, suggesting that the self-reports in this group might be accurate.23 However, the MMSE is a poor preTABLE 2.
dictor of other forensic capacities, such as the capacity to give informed consent.24 In contrast, EXIT25 scores are strongly associated with a variety of forensic capacities, including the capacity to make an advance directive and the capacity to give informed consent for medical care.11,25,26 Eighteen percent of the comparison subjects had EXIT25 scores indicating impairment, although persons similar to the comparison subjects—siblings and spouses of hospitalized patients—are frequently asked to provide substituted consent or ancillary history for incapacitated patients on medical inpatient wards. We report on the prevalence of executive impairment
Admission Cognitive Test Scores of Patients Hospitalized on a General Medicine Service and Nonhospitalized Comparison Subjectsa Nonhospitalized Comparison Subjects
Hospitalized Patients Test Executive Interview (EXIT25) Executive Clock Drawing Task (CLOX) CLOX1 CLOX2 Mini-Mental State Examination
Analysis
N
Median
95% CI
N
Median
95% CI
z
p
100
13
11–15
50
9.5
8–12
ⳮ2.32
0.02
99 99 100
12 13 28
12–12 13–14 28–28
50 50 50
11–13 13–14 29–30
0.75 1.01 2.60
12 14 29
0.45 0.31 0.009
a Patients were tested within 24 hours of admission; nonhospitalized comparison subjects, who were siblings and spouses of the patients, were tested during the course of the patients’ hospitalization.
TABLE 3.
Cognitive Test Scores at Admission and Discharge of Patients Hospitalized for ⱖ2 Days on a General Medicine Service Admission
Discharge
Analysis
Test
N
Median
95% CI
N
Median
95% CI
z
p
Executive Interview (EXIT25) Executive Clock Drawing Task (CLOX) CLOX1 CLOX2 Mini-Mental State Examination
60
11
9–16
38
11
6–14
ⳮ1.56
0.11
59 59 60
12 13 28
11–12 13–14 27–29
38 38 38
13 14 29
12–14 13–14 28–29
3.94 1.70 1.20
TABLE 4.
⬍0.001 0.09 0.23
Admission Executive Interview (EXIT25) Scores of Patients in Various Diagnostic Categories Hospitalized on a General Medicine Service and Nonhospitalized Comparison Subjects Analysisa
EXIT25 Score Group and Diagnostic Category
N
Median
95% CI
z
p
Hospitalized patients Cancer Cardiac disorder Endocrine disorder Gastrointestinal disorder Infection Pulmonary disorder Other Nonhospitalized comparison subjects
10 7 6 15 31 14 17 50
14.5 17 16 14 12 10 11 9.5
4–28 9–25 6–20 9–21 7–16 6–14 8–16 8–12
1.50 2.01 1.73 2.60 1.31 0.29 1.02 —
0.13 0.04 0.08 0.01 0.19 0.78 0.31 —
a
For comparison of hospitalized patients and nonhospitalized comparison subjects.
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Executive Impairment as measured by the EXIT25 and CLOX1. Although 52% of the patients scored in the range indicating impairment on one or the other of these measures, these measures may not represent a comprehensive assessment of executive function, which has multiple dimensions.27 We observed a high degree of overlap in the patients identified as executively impaired by these measures, and it is possible that the addition of other measures of executive function might have further increased the prevalence of executive impairment, relative to the prevalence we report. However, such findings would only strengthen our conclusion that executive impairment is common among medical inpatients. Executive impairment may improve through the course of usual standard-of-care medical management, but further study of this outcome is needed. Fifty-six percent of the patients in our study were discharged back to the community after having scored in the range indicating impairment on at least one measure of executive function within the previous 24 hours. This high rate of executive impairment probably was not detected by clinicians, as only 4% of the patients scored below the MMSE cutoff score for impairment within 24 hours of discharge. Furthermore, some patients may be discharged with worse ex-
ecutive function than they had at admission, as evidenced by our finding that 5% of the patients with an EXIT25 score indicating impairment at discharge had a score within the normal limits at admission. We conclude that as many as one-half of medical inpatients are vulnerable to executive impairment. The MMSE is insensitive to this impairment and should not be used as the sole cognitive screening test in this setting. Executive impairment may undermine the quality of information obtained from patients, undermine attempts to obtain informed consent for treatment, undermine treatment adherence, and complicate efforts to discharge patients safely. Moreover, a significant fraction of the caregivers available to assist in these matters may have similar impairments. Further study is warranted to confirm our findings and further explore medical risk factors for executive impairment. This project was funded in part by an unrestricted educational grant from the Department of Psychiatry of the University of Texas Health Science Center at San Antonio. The first author received the American Psychiatric Association/Lilly Resident Research Award for this body of work.
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