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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 61:1307-1311 (2006)
© 2006 The Gerontological Society of America

SPECIAL SECTION

Does Educational Attainment Contribute to Risk for Delirium? A Potential Role for Cognitive Reserve

Richard N. Jones, Frances M. Yang, Ying Zhang, Dan K. Kiely, Edward R. Marcantonio and Sharon K. Inouye

1 Institute for Aging Research, Hebrew SeniorLife, Boston, Massachusetts.
2 Division of Gerontology and 3 General Medicine and Primary Care, Beth Israel Deaconess Medical Center, Boston, Massachusetts.
4 Department of Psychiatry, Division of General Medicine, Brigham and Women's Hospital, Boston, Massachusetts.
5 Harvard Medical School, Cambridge, Massachusetts.

Address correspondence to Richard N. Jones, ScD, Institute for Aging Research, Hebrew SeniorLife, 1200 Centre St., Boston, MA 02131. E-mail: jones{at}mail.hrca.harvard.edu


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. The objective of this study was to determine if level of educational attainment, a marker of cognitive reserve, was associated with the cumulative risk of delirium among hospitalized elders.

Methods. We performed a secondary analysis of two hospital-based studies. The first (study 1) was an observational study involving 491 admissions. The second study (study 2) involved consecutive admissions assigned to the usual care condition in a controlled clinical trial, and included 461 persons. All participants were elderly (aged 70+) and free from delirium at admission. The outcome was the occurrence of delirium, as rated by the Confusion Assessment Method during hospitalization.

Results. In study 1 and 2, 22% and 14% of persons developed delirium (cumulative incidence), respectively. In both studies, risk of delirium was higher among persons with fewer years of education. Controlling for the effect of age, sex, dementia, comorbidity, and severity of illness, each year of completed education was associated with a 0.91 lower odds of delirium (95% confidence interval: 0.87, 0.95): compared to persons with 12 years of education, persons with 7 years of education had 1.6-fold increased odds of delirium (95% confidence interval: 1.4, 2.0).

Conclusion. Hospitalized older persons with low educational attainment are at increased risk for delirium relative to persons with more education. This finding may have implications for the role of cognitive reserve in characterizing individual differences in risk for delirium.

DELIRIUM, or acute confusional state, is common among hospitalized older adults. It occurs frequently after surgical procedures, complicates recovery, and forestalls return to previous level of functioning (1,2). Delirium contributes to worse functional outcomes among older patients with dementia (2); however, research to date has yet to establish whether delirium leads to dementia. Inouye notes that, although delirium and dementia have traditionally been considered two separate conditions, their clinical and pathophysiologic overlap suggests that they may represent two ends of a spectrum (2). Targeting delirium can improve the understanding of cognitive disorders and dementias and provide a means for early detection and treatment. Addressing the role of cognitive reserve in delirium may improve our understanding of the mechanisms of and interventions for the preservation of cognitive reserve (2).

The concept of reserve has been cited as a theoretical framework for explaining individual differences in risk for, and patterns of, cognitive impairment associated with dementia (3–5), brain injury, or medical illness (3). Reserve has been suggested to account for individual differences in risk for delirium (6). Reserve is a generic term that refers to passive and active processes in the brain that modify an individual's risk for expression of clinical signs and symptoms associated with brain injury or neuropathology. The key concept in passive reserve models, also referred to as brain reserve or threshold, is that there are individual differences in the amount of damage that the brain can endure before reaching a critical threshold for clinical expression (7). Differences are caused by structural features such as brain size and synapse density (4). An active model of reserve, cognitive reserve, refers to the degree of efficiency with which an individual uses relevant brain networks or cognitive strategies to cope with brain injury (as indicated by brain pathology, impaired neuropsychological performance, or clinical signs of dementia). Markers have been suggested to include educational attainment, occupational achievement, and intelligence (4). Among the markers of cognitive reserve, educational attainment may be the most widely studied. The strong and robust association of educational attainment with risk for dementia has led some investigators to claim that education may be the most important risk factor for dementia (7). However, the relationship between educational attainment and delirium has been poorly examined to date.

In a comprehensive review from 1998, Elie and colleagues (8) identified only one study that considered educational attainment as a risk factor for delirium; however, this study did not actually present any primary data on education (9). More recently, two studies have identified educational attainment as an important risk factor for delirium. In a prospective cohort of older persons, Galanakis and colleagues identified low educational (e.g., elementary education only) as a risk factor for delirium (odds ratio [OR] = 3.6, 95% confidence interval [CI]: 1.1–11.2), with a moderate-to-large-effect size difference (10,11). In a prospective cohort of 432 medical and surgical patients, Pompei and colleagues (12) found that patients with delirium were less likely than those without delirium to have completed some education beyond the 12th grade (22% vs 30%). This effect was statistically significant but demonstrated only a modest effect size difference (11). By contrast, at least three previous studies have failed to demonstrate a significant effect of education on the risk of delirium (13–15).

The goal of the present study was to extend the previous work and to further examine the role of educational attainment in two previous large prospective cohort studies (16,17). These studies included assessment of educational level by year, along with frequent clinical assessments for delirium throughout hospitalization. We hypothesized that individuals with higher education would be less likely to experience incident delirium during their hospital stay.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
Sample
The design and sampling framework for the two studies, reported in detail previously (16–18), will be briefly summarized. The most common diagnoses for the hospitalized elders potentially eligible to participate in the study were congestive heart failure, anemia, pneumonia, and chronic obstructive disease. Eligibility criteria differed slightly for each study but included having an age of at least 70 years, and the absence of a delirium diagnosis based on an algorithm operationalized within the Confusion Assessment Method (CAM) (19).

Study 1.-- This study accrued a sample of 491 medical patients aged 70 and older admitted to an acute care hospital in the New Haven, Connecticut, area from November 1989–July 1991. Terminal illness and refusing to provide consent were among the exclusion criteria. Additional details can be found in previous reports (17,18). Patients were evaluated at admission and discharge and every other day during their hospital stay for the presence of delirium using the CAM criteria (19). The outcome for this analysis is the presence of CAM delirium at any point during the hospital stay (17).

Study 2.-- This study was a controlled clinical trial of a multicomponent delirium prevention strategy (16). In this analysis, we consider only 421 persons admitted to units randomized to the usual care and control condition of an urban teaching hospital in the New Haven area between March 1995 and April 1998. Eligible persons were aged 70 years or older and admitted to the general medicine service. This sample represents a true prospective cohort of consecutive admissions. Profound dementia, aphasia, language barrier, intubation or respiratory isolation, coma or terminal illness, and stays of less than 48 hours were among the exclusion criteria. Additional details can be found in Inouye and colleagues (16). Patients were assessed daily until discharge for the presence of delirium using cognitive assessment and the CAM instrument (16). As in study 1, in this analysis we use the occurrence of any CAM delirium during the hospital stay as the outcome variable.

In both studies, informed consent for participation was obtained from the patient, or, for those with significant cognitive impairment, from the closest relative or legal guardian, according to procedures approved by the institutional review board of Yale University School of Medicine.

Delirium Assessment
Trained clinical interviewers conducted structured interviews with the patients from hospital admission until discharge, which included cognitive assessment using the Mini-Mental State Examination (20) and delirium rating using the CAM (19). Delirium was defined according to the presence of the CAM criteria, which consisted of acute onset and fluctuating course, inattention, and either disorganized thinking or altered level of consciousness. Each of these features was rated by the interviewers based on observations made during their structured interviews and cognitive assessment. The CAM criteria provided a standardized rating for delirium, which has been validated against geropsychiatric diagnoses, with a sensitivity of 94%–100% and specificity of 90%–95% (19). We also considered the severity of delirium, which was measured by an additive score of 0–7 for the four CAM symptoms: symptom fluctuation (scored 0–1), inattention (scored 0–2), disorganized thinking (scored 0–2), and altered level of consciousness (scored 0–2) (16). Higher scores indicated increasing severity.

Educational Attainment
Information on educational attainment was collected from the patients during baseline interviews conducted within 48 hours of hospital admission. Patients were asked to report on the total years of formal education that they had completed. Educational attainment was treated as a continuous variable in our multivariable regression models, capturing years of education. We also presented graphical summaries of educational attainment group categorized discretely (Figure 1): less than 7 years (elementary), 7 to 12 years (middle to high school), 13 to 16 years (college), more than 16 years (graduate school). In studies 1 and 2, respectively, 19 and 3 patients had missing information on educational attainment. These persons were included in the analysis and placed in the lowest education level, since they often had no formal education in the United States. Two alternative methods for handling this missing information were explored [singly imputing the mean and a complete data maximum likelihood estimation methods (21) assuming a normal distribution of educational attainment.]


Figure 01
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  		Figure 1. Risk of delirium during hospitalization as a function of level of educational attainment in two studies of consecutive hospital admissions

 
Other Study Variables
We included age (in years divided by 10 in analytic models), men (vs women), the presence of dementia [defined as the presence of a diagnosis of dementia or a modified Blessed Dementia Rating scale (22) score of 4 or higher), comorbidity indexed with the Charlson comorbidity score (23), and the Acute Physiology and Chronic Health Evaluation score as a marker of severity of illness (24)] (standardized in our regression models) as control variables in our multivariable models.

Analytic Approach
We used logistic regression to test whether differences in the cumulative risk of delirium during the hospitalization was related to level of educational attainment, controlling for variables known to be risk factors for delirium (16). Because our interest was in whether, rather than when, an older person might experience delirium during hospitalization, we used logistic regression rather than a time-to-event analysis framework.


   RESULTS
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 Methods
 Results
Discussion
 References
 
Participant characteristics are presented in Table 1. Both studies accrued very old, predominantly female and white, non-Hispanic samples. Differences in the proportion among the oldest-old, male, and white, non-Hispanic level of comorbidity and prevalence of dementia were not significant across the studies.


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  		Table 1. Characteristics of Participants From Two Studies of Delirium During Hospitalization.

 
In study 1, 106 of 491 (22%) of persons developed delirium during their hospitalization. The mean (standard deviation, SD) years of education among persons who developed delirium was 9.3 (4.7) years, compared to 11.3 (3.8) years among those who did not. In study 2, 63 of 461 persons (14%) developed delirium. The mean (SD) years of education among those who developed delirium was 9.4 (3.9) years, relative to 11.2 (3.7) years among those who did not. Both of these differences were statistically significant (p <.001) and describe approximately medium-sized effects in Cohen's (11) effect size taxonomy (d =.48, d =.51, respectively).

The relationship of cumulative incidence of delirium and level of educational attainment collapsed into discrete groups is summarized in Figure 1. This figure displays the proportion with delirium during their hospitalization, with 95% confidence bands, and a fitted trend line, as a function of level of grouped educational attainment. In both studies, there is a decreasing trend for the occurrence of delirium with increasing years of education. The trend lines imply statistically significant linear trends, which were tested and confirmed in the multivariable logistic regression models (Table 2).


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  		Table 2. Regression Models of Cumulative Risk of Delirium on Educational Attainment and Control Variables.

 
Table 2 contains the results of regression models testing the linear effect of years of education as a predictor of cumulative delirium risk during the hospitalization. For each study, results of two models are presented. Model 1 displays the bivariable regression of the occurrence of delirium on years of education, and model 2 displays the result including the control variables (multivariable models).

In bivariable analysis (model 1), years of completed education is a statistically significant (p <.001) predictor of delirium in both studies, with nearly equivalent effect estimates. When statistical control is added for age, male sex, dementia, comorbidity, and disease severity, the effect of education is attenuated but remains statistically significant in both studies (p <.001). The reduction in the regression coefficient in the multivariable models is approximately 28% and 18% in study 1 and 2, respectively. This change reflects a potentially clinically significant level of confounding (25) or mediation (26) of the effect of education by the control variables, most likely dementia and level of comorbidity. In the pooled analysis, each year of education was associated with less cumulative risk of delirium (OR = 0.91, 95% CI: 0.87–0.95). To gauge the effect of a 5-year difference in educational attainment (the interquartile range), such as completing grade 7 versus grade 12, one can compute e5xln(OR–1), which returns a 1.6-fold increase in the odds of delirium for patients with a middle school education versus a high school education (95% CI 1.3, 2.0).

Finally, we examined two alternative methods for handling missing data in the education variable. The first was a single mean imputation, and the second a maximum likelihood estimation method that uses all available information. For both of these methods, the resulting OR for a 5-year difference in education was approximately equal (OR = 1.5) and slightly attenuated relative to the one estimated with the zero imputation (OR 1.6). However, in both sensitivity analyses, the OR without the zero imputation remained statistically significant.

To further probe the relationship of education and delirium, we conducted two supplementary analyses. First we examined if, among persons who developed delirium, the severity of delirium was associated with level of educational attainment. For these analyses, involving only patients with delirium, we collapsed patients into a high and low education group (splitting at 12 years) due to small sample sizes. Among persons with incident delirium, there was no difference between persons who had completed 12 or fewer years of education versus more education in terms of delirium severity in study 1 [mean (SD) severity 3.4 (1.3) vs 3.5 (1.3), p =.70)] and in study 2 [mean (SD) severity 3.7 (1.0) versus 4.2 (1.6), p =.24].

Our second supplementary analysis involved investigating the possibility of effect modification of the education–delirium relationship with respect to dementia. We investigated this two ways. First, we repeated our logistic regression models (Table 2) stratifying by the presence of dementia. We also performed a logistic regression analysis that included a dementia by education interaction. Results of the stratified analyses revealed that education was associated with an increased cumulative risk of delirium in all strata. In the model with the interaction term, the interaction term indicated that the relationship between educational attainment and risk of delirium was not significantly different between persons with and without dementia (p =.55). These supplementary models suggest dementia is not an effect modifier of the relationship between educational attainment and risk for delirium.


   DISCUSSION
Top
 Abstract
 Methods
 Results
 Discussion
References
 
Our results support the hypothesis that higher education is associated with a lower cumulative incidence of delirium. Each year of education was equivalent to about 1.7 (study 1) to 2.9 (study 2) years of age in terms of accounting for cumulative delirium risk. In one study (study 2), the excess risk associated with a 6-year difference in education was equivalent to the presence of dementia.

Some limitations of our analysis deserve comment. Our samples are drawn from urban areas around New Haven, Connecticut, and may not be generalizable to other populations. Our studies were performed in the 1980s and 1990s, and the meaning, quantity, and quality of education for the cohort of older adults at that time may not be equivalent to that of current and future cohorts. We do not include information about psychoactive pharmacotherapies or lifestyle factors (e.g., intellectually stimulating activities, occupation). Finally, our sample was underpowered to detect differences in delirium severity among those with delirium. The strengths of this study include the prospective data collection, a sensitive education variable and state-of-the-art delirium assessment, and replication of our findings across two independent samples.

Dementia is a leading risk factor for delirium (2). However, we have shown that, independent of the effect of dementia, education is associated with delirium risk. Delirium may be the manifestation of low reserve and thereby serve to identify persons at greater risk of dementia. Delirium and dementia may share pathophysiologic mechanisms (decreases in cerebral metabolism, anticholinergic activity, and inflammation) (2). Therefore, while the disease processes underlying dementia (Alzheimer's type, Lewy body type, and so forth) may be distinct from those of delirium [which are poorly understood, see (2)], individual vulnerability to the underlying processes may be modified by a common substrate. This common substrate fits the theory articulated in the reserve model, and would include theoretical constructs such as cognitive reserve, brain reserve, and compensation as described by Stern and his colleagues (5).

To more clearly delineate the role of reserve in delirium and dementia risk, we propose a generalization of a research paradigm for investigating the role of reserve markers (education, intelligence) and dementia. This paradigm is illustrated in Figure 2. Evidence for reserve is derived from demonstrating a modification of the effect of pathophysiologic markers of disease staging (e.g., burden of neuritic plaques, neurofibrillary tangles) or known risk factors (e.g., apolipoprotein E [APOE] genotype) for dementia or cognitive decline by a marker of reserve (e.g., education). Our proposed generalization of this paradigm includes linking a neurotoxic exposure (e.g., surgery) to the occurrence of delirium and consequently to the development of dementia. We expand the reserve concept to include multiple indicators of reserve, including sociodemographic, social–behavioral, psychometric, and biometric indicators. A multiple indicator measure of reserve has been suggested previously that incorporates sociodemographic and psychometric indicators (27). Our expansion to biometric indicators includes quantitative magnetic resonance imaging measures of brain reserve have been proposed (providing evidence of differences in the quantity of brain matter), and new emerging protocols for eliciting measures of cognitive reserve using functional magnetic resonance imaging and cognitive activation protocols (27–29). APOE genotype is also a potential indicator of reserve: Scarmeas and colleagues (30) have shown that even among college-aged and neurologically normal adults, APOE genotype is associated with variations in cerebral activation patterns.


Figure 02
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  		Figure 2. A generalized reserve theory experimental design linking neurotoxic event or exposure, delirium, and dementia, and expanding the reserve concept. [See text for full description of annotations.] qMRI = quantitative magnetic resonance imaging; fMRI = functional magnetic resonance imaging; APOE = apolipoprotein E genotype; WAIS = Wechsler Adult Intelligence Scale; NART = National Adult Reading Test

 
Our current research offers insight into a very limited aspect of the proposed reserve–delirium–dementia pathway. The questions we have addressed are shown in solid lines in Figure 2. Unanswered questions remain and are illustrated with broken lines. Key to the reserve hypothesis are paths labeled 3 and 4: the modification of the effect of known toxic events or risk factors and the occurrence of clinically relevant outcomes (delirium and dementia). We view the present work as the initiation of a line of research linking social science and epidemiologic approaches with clinical and mechanistic models for delirium risk and for addressing questions concerning delirium progressing to dementia.


   Acknowledgments
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 Abstract
 Methods
 Results
 Discussion
 References
 
Funded in part by grants from the National Institute on Aging (R01AG17649, R03AG025262, R01AG025308, P60AG008812, R21AG025193, and K24AG00949). Additional support was provided by the Education Core of the Massachusetts Alzheimer's Disease Research Center (P50AG005134), a conference grant from the Alzheimer's Association, and the Aging Brain Center, Institute for Aging Research, Hebrew SeniorLife.

Dr. Marcantonio is a Paul Beeson Physician Faculty Scholar in Aging Research.


   Footnotes
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 Abstract
 Methods
 Results
 Discussion
 References
 
Decision Editor: Luigi Ferrucci, MD, PhD

Received July 3, 2006

Accepted September 11, 2006


   References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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S. K. Inouye and L. Ferrucci
Introduction: Elucidating the Pathophysiology of Delirium and the Interrelationship of Delirium and Dementia
J. Gerontol. A Biol. Sci. Med. Sci., December 1, 2006; 61(12): 1277 - 1280.
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