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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 61:736-742 (2006)
© 2006 The Gerontological Society of America

Total Serum Cholesterol and Recovery From Disability Among Hospitalized Older Adults

Graziano Onder, Stefano Volpato, Rosa Liperoti, Carola D'Arco, Cinzia Maraldi, Renato Fellin, Roberto Bernabei, Francesco Landi, on Behalf of the GIFA Investigators

1 Department of Geriatrics, Catholic University of the Sacred Heart, Rome, Italy.
2 Second Department of Clinical and Experimental Medicine, University of Ferrara, Italy.
3 Department of Aging and Geriatric Research, University of Florida, Gainesville.

Address correspondence to Graziano Onder, MD, Centro Medicina dell'Invecchiamento, Università Cattolica del Sacro Cuore, Policlinico A. Gemelli, L.go F. Vito 1, 00168 Rome, Italy. E-mail: graziano_onder{at}rm.unicatt.it


   Abstract
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 Abstract
Methods
 Results
 Discussion
 References
 
Background.The association between total serum cholesterol and health outcomes among older adults is controversial. The objective of the present study was to determine within a cohort of acutely hospitalized disabled elderly patients whether total cholesterol predicts recovery from disability in basic activities of daily living (ADL).

Methods.Patients (3150) 65 years old or older admitted to 81 acute care units in Italy and presenting with ADL disability at hospital admission were included in this study. ADL disability was defined as need of assistance or total dependence in one or more ADLs (eating, dressing, personal hygiene, transferring, and toilet use). Recovery was defined as no disability at hospital discharge in any of the five ADLs considered.

Results.Mean age of study participants was 80.5 ± 7.2 years, and 1305 (41.1%) were men. The rate of recovery from ADL disability was 14.5% for participants with total cholesterol <200 mg/dL (n = 306/2108), 20.2% for those with total cholesterol between 200 and 239 mg/dL (n = 144/713), and 23.1% for those with total cholesterol ≥240 mg/dL (n = 76/329). After adjustment for potential confounders, relative to that of patients with cholesterol <200 mg/dL, risk ratios for recovery were 1.31 for participants with cholesterol between 200 and 239 mg/dL (95% confidence interval [CI], 1.07–1.62) and 1.36 (95% CI, 1.04–1.79) for those with cholesterol ≥240 mg/dL. After exclusion of 769 patients with total cholesterol <145 mg/dL, the risk ratios (compared with those for participants with cholesterol <200 mg/dL) for recovery were 1.33 (95% CI, 1.07–1.66) for participants with cholesterol between 200 and 239 mg/dL and 1.41 (95% CI, 1.06–1.88) for patients with cholesterol ≥240 mg/dL.

Conclusions.Among hospitalized disabled older adults, elevated levels of cholesterol are associated with increased rate of recovery from ADL disability.

DESPITE considerable evidence suggesting that, in young and middle-aged individuals, serum cholesterol is directly associated with an increased risk of adverse health outcomes, including long-term mortality, the importance of elevated cholesterol levels as a risk factor for adverse outcomes in older adults is still controversial (1–6). A major difference between middle-aged and older adults is the prevalence of co-existing diseases and consequent poor health in the latter group (7). Older persons with a high burden of disease may have low cholesterol levels, as compared to those with few (or no) medical comorbidities who have low-to-normal cholesterol levels (8). Indeed, total cholesterol levels tend to decrease among older persons, both in men and in women, and this trend may relate, to a great extent, to the effects of poor health (9). Thus, poor health appears to confound the relationship between cholesterol levels and adverse outcomes in older patients.

Interestingly, a recent study showed that, in a population of high-functioning older adults, after adjusting for potential confounders, including markers of poor health, increments in non-high-density lipoprotein cholesterol were associated with a lower risk of developing disability in activities of daily living (ADLs) (10). This finding is consistent with a previous observation in a cohort of older adults indicating that high levels of total cholesterol were associated with a decreased risk of physical disability after stroke (11).

Among older adults, the inability to perform basic ADLs is common, highly morbid, and costly. In addition, it leads to adverse outcomes, including mortality and nursing home admission, and to an increased burden of care for formal and informal caregivers (12–16). The disability process is often the result of a progressive breakdown of the homeostatic equilibrium, described as a complex sequence of events in which multiple chronic diseases play an important role (17). However, some older persons may become disabled suddenly, as a consequence of a catastrophic event, such as a stroke or a hip fracture, without showing any previous sign of functional decline (18). In this context, hospitalization secondary to acute illness or injuries represents an important source of disability for older persons living in the community, accounting from 50% to 80% of cases of disability (19,20).

In addition, disability has usually been considered a simple, static condition, whereas (particularly among physically frail older adults) it is a highly dynamic process with considerable heterogeneity (21–25). Longitudinal studies have found that a substantial proportion of elderly persons, after becoming disabled, recover independence in ADL function, suggesting that the disabling process among many older persons is complex, with multiple and possibly interrelated disability episodes, even over relatively short periods of time (23–25).

So far, only few studies have assessed the impact of total serum cholesterol levels on ADL recovery, particularly in the short term and among older persons admitted to hospital. Therefore, the aim of the present study is to determine within a cohort of disabled elderly patients hospitalized for an acute medical event whether total serum cholesterol predicts recovery from ADL disability, independent of comorbidity and other indicators of health status.


   METHODS
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The GIFA (Gruppo Italiano di Farmacoepidemiologia nell'Anziano), a group of investigators who are based in acute care units of university and community hospitals throughout Italy, periodically surveys drug use, occurrence of adverse drug reactions, and quality of hospital care.

GIFA Database
The methods of GIFA have been described in detail elsewhere (9,26). Briefly, all patients admitted to 81 clinical centers in Italy were enrolled and followed until discharge. The study periods were May 1 to June 30 and September 1 to December 31, 1988; May 15 to June 15, 1991; and May 1 to June 30 and September 1 to October 31 in 1993, 1995, 1997, and 1998.

For each participant, a questionnaire was completed at admission and updated daily by a study physician who had received specific training. Data collected included demographic characteristics, functional and cognitive status, medications taken prior to admission and during hospital stay, and admission and discharge diagnoses.

Laboratory Parameters
As previously described, clinical chemistry test results, including total serum cholesterol, were collected during the 1993, 1995, 1997, and 1998 survey periods (9,26). Total cholesterol was part of a series of blood tests that were routinely done at admission. Data on cholesterol subfractions such as low-density lipoprotein (LDL) and high-density lipoprotein (HDL) were not gathered. All routine laboratory tests were performed the morning after the first day of admission, following an overnight 12-hour fast. Samples were assayed, using standardized enzymatic methods, in the central laboratory at each clinical center. Each laboratory fulfilled the requirements of a standard quality control program, thus ensuring the reliability and validity of all biochemical measures. For analytic purpose, and in line with indications of The Adult Treatment Panel III (ATP III; 27), three groups of total cholesterol were defined: group 1 = <200 mg/dL (desirable cholesterol), group 2 = 200–239 mg/dL (borderline high cholesterol), and group 3 = ≥240 mg/dL (high cholesterol).

Serum albumin was measured using the colorimetric method. A cutoff of 3.5 g/dL was used to compute a two-level variable for this parameter. Erythrocyte sedimentation rate (ESR) after the first hour was measured by the Westergren method. A cutoff of 30 mm/h was used to compute a two-level variable for this parameter.

ADL Assessment
Functional status was evaluated by self-report information including five basic ADLs (personal hygiene, transferring from bed to chair, using the toilet, dressing, and eating). Patients or proxy were interviewed at the time of hospital admission and hospital discharge. Data on proportion of assessments completed by proxy were available only in the 1998 survey. In this study period, information on functional status was provided by proxies in 50% of cases.

For each ADL, at hospital admission and discharge, participants (or proxies) were asked, "What kind of assistance or help do(es) you (he or she) need to perform the task?" For every activity the level of dependency at hospital admission and discharge was coded as follows: independent (no help or oversight needed), supervision (oversight, encouragement, or cueing needed), limited assistance, intensive assistance, or total dependency. ADL disability was defined as need of assistance or total dependence in one or more tasks. Only persons with ADL disability at hospital admission were considered eligible for this study. The outcome of this study was recovery from ADL disability, defined as no disability at hospital discharge in any of the five ADLs considered.

Covariates
Covariates include sociodemographic and clinical characteristics. Age was categorized as 65–79 years old or 80 years old or older. Cognitive performance was assessed using the Hodkinson Abbreviated Mental Test. Based on a previous observation in an Italian population, a score <7 defined cognitive impairment (28). Drugs were coded according to the Anatomical Therapeutic and Chemical codes (29). Discharge diagnoses were coded according to the International Classification of Diseases, Ninth revision, Clinical Modification codes (30). Comorbidity was quantified using the Charlson comorbidity index by adding scores assigned to specific discharge diagnoses, as illustrated in the original publication (31). Body mass index (BMI) (kg/m2) was calculated using objective measures, and was coded as a three-level variable, using the cut points 18.5 and 25 kg/m2. Number of hospital admissions in the year prior to hospitalization and residential status before admission were self-reported. Number of impaired ADL at hospital admission was defined as the number of ADL for which assistance was required.

Study Sample
For the present analysis, we considered only patients 65 years old or older who had been admitted during the 1993, 1995, 1997, and 1998 survey periods, and for whom laboratory parameters had been recorded. From an initial sample of 11,586 participants 65 years old or older, in whom clinical chemistry data had been collected, we excluded 165 persons lacking ADL assessment at hospital admission and 2159 patients for whom BMI data had not been collected. In comparison to persons excluded from study participation due to incomplete data, those included in the study were significantly younger (78 ± 7 vs 80 ± 7 years, p <.001), less likely to be cognitively impaired (Hodkinson abbreviated mental test <7: 32% vs 50%, p <.001) and had fewer comorbid conditions (Charlson comorbidity index ≥2: 43% vs 47%, p =.003), a lower rate of ADL disability at hospital admission (37.1% vs 59.6%, p <.001), and a higher level total cholesterol (185 ± 50 vs 179 ± 53 mg/dL, p <.001).

As shown in Figure 1, in the resulting sample of 9263 participants, 3438 (37.1%) presented with ADL disability at hospital admission. Among these latter participants, 526 (15.3%) recovered their ADL function, 2624 (76.3%) remained disabled in at least one ADL, 269 (7.8%) died during hospital stay, and 19 (0.6%) were lacking ADL assessment at discharge. Among participants with ADL disability at hospital admission, those dying during hospital stay had a lower total cholesterol level than did the other participants (165 ± 56 vs 179 ± 49 mg/dL, p <.001). Participants dying during hospital stay and those lacking ADL assessment at discharge were excluded from the study, leading to a final study sample of 3150 patients.


Figure 01
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  		Figure 1. Study profile. Activity of Daily Living (ADL) disability was defined as need of assistance or total dependence in one or more of the following tasks: eating, dressing, personal hygiene, transferring, and toilet use. Recovery was defined as no disability at hospital discharge in any of the five ADLs considered

 
Data Analysis
To compare baseline characteristics across study groups, analysis of variance was performed for continuous variables. Chi-square analysis was used for dichotomous variables. Outcome of the study was recovery from ADL disability, defined as requiring no assistance in any of the five ADLs considered at hospital discharge.

Crude and adjusted risk ratios (RRs) and 95% confidence intervals (CIs) for ADL recovery in different cholesterol groups were calculated using modified Poisson regression models for prospective studies with binary data as suggested by Zou (32). Variables considered for adjustment were those considered clinically relevant or associated with recovery from ADL disability at p ≤.10 at the univariate analysis. We included in the model age, gender, number of ADLs impaired at hospital admission, cognitive impairment, Charlson comorbidity index, BMI, albumin level, ESR, stroke, cancer, congestive heart failure, liver disease, diabetes, length of hospital stay, number of drugs used during hospital stay, use of lipid-lowering drugs, use of angiotensin-converting enzyme inhibitors, residential status, number of hospital admissions in the last year, and year of survey. In additional regression models we explored the effect of total cholesterol levels on ADL disability recovery in participants: (i) with total cholesterol above the 25th percentile (total cholesterol ≥ 145 mg/dL) and in participants (ii) presenting with diabetes, ischemic heart disease, or cerebrovascular disease. Statistical analysis was performed using SPSS (version 10.1; SPSS Inc., Chicago, IL) and SAS (version 8; SAS Institute Inc., Cary, NC) software.


   RESULTS
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Discussion
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The mean age of the 3150 patients with ADL disability at hospital admission included in the study was 80.5 ± 7.2 years, 1305 (41.1%) were men, and the mean length of hospital stay was 15.8 ± 10.9 days. The mean value of total cholesterol was 179 ± 49 mg/dL (range: 50–492 mg/dL), and 526 participants (16.7%) recovered from ADL disability (meaning that they required no assistance in any ADL at hospital discharge).

The distribution of demographic, functional, clinical, and biochemical characteristics according to recovery from ADL disability at hospital discharge is presented in Table 1. Recovery from ADL disability was inversely associated with increasing age, number of impaired ADLs at hospital admission, cognitive impairment, Charlson comorbidity index, number of hospital admissions in the last year, indicators of poor nutritional status (low BMI and albumin < 3.5 gr/dL), and ESR, whereas an direct association was observed with length of hospital stay, number of drugs used during hospital stay, and use of lipid-lowering drugs and angiotensin-converting enzyme inhibitors. Among specific medical conditions, stroke and cancer were associated with a lower recovery rate from ADL disability, whereas patients with congestive heart failure, liver disease, or diabetes were more likely to regain complete independence.


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  		Table 1. Bivariate Comparison of Principal Characteristics of the Population (N = 3150) According to Recovery From ADL Disability.

 
Mean total cholesterol was 188 ± 53 mg/dL among participants recovering from ADL disability as compared to 178 ± 48 mg/dL among those not recovering (p <.001). As shown in Table 2, the rate of recovery from ADL disability was 14.5% in patients with total cholesterol <200 mg/dL (n = 306/2108), 20.2% in those with total cholesterol between 200 and 239 mg/dL (n = 144/713), and 23.1% for those with total cholesterol ≥240 mg/dL (n = 76/329). In the unadjusted model, total cholesterol was positively associated with recovery from ADL disability. After adjusting for potential confounders, the strength of the association between total cholesterol level and recovery from ADL disability was slightly attenuated, but still substantial, and statistically significant: Relative to patients with cholesterol <200 mg/dL, RRs for recovery were 1.31 for participants with cholesterol between 200 and 239 mg/dL (95% CI, 1.07–1.62) and 1.36 (95% CI, 1.04–1.79) for those with cholesterol ≥240 mg/dL. Compared with participants with cholesterol between 200 and 239 mg/dL, RR of recovery of participants with cholesterol ≥240 mg/dL was 1.04 (95% CI, 0.78–1.38). After exclusion of 769 patients with total cholesterol <145 mg/dL, the RRs (compared with that of participants with cholesterol <200 mg/dL) for recovery were 1.33 (95% CI, 1.07–1.66) for participants with cholesterol between 200 to 239 mg/dL and 1.41 (95% CI, 1.06–1.88) for patients with cholesterol ≥240 mg/dL. Similarly including in the regression model only participants presenting with prevalent diabetes, ischemic heart disease, or cerebrovascular disease, cholesterol ≥ 200 mg/dL was still associated with an increased probability of recovery. In the fully adjusted model, no significant interaction was observed between presence of one or more of these conditions and total cholesterol on recovery from ADL disability (p for interaction =.72). In addition, no significant interaction was observed between age and total cholesterol on study outcome (p for interaction =.50).


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  		Table 2. Association of Total Cholesterol Levels With Recovery From ADL Disability.

 

   DISCUSSION
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References
 
To our knowledge, this report represents the first study to assess the relationship between cholesterol and recovery from ADL disability in the short term among acutely ill hospitalized patients. The present study shows that nearly 15% of patients presenting with ADL disability at admission regain their ADL independence at discharge and that serum cholesterol ≥200 mg/dL is associated with an increased probability of recovery, regardless of malnutrition, inflammation, and comorbidity. This result was consistent after exclusion of persons with a very low level of total cholesterol or including in the analysis only participants with cardiovascular disease or diabetes.

The rate of recovery from ADL disability in our study is lower than those observed in the long term among older adults living in the community, but it confirms the idea that disability is a highly dynamic process and that ADL function can widely change even in the short term and among older adults experiencing an acute condition (21–25). Interestingly, Gill and colleagues (20) have shown that illnesses and injuries leading to hospitalization represent an important source of disability for older persons living in the community, and Verbrugge and colleagues (33) demonstrated that physical function improves in the first month after hospitalization, and then fluctuates substantially in the following months. This concept clearly refutes the perception that disability leads invariably to further decline in physical function and increasing dependence.

The relationship between cholesterol and recovery from ADL disability confirms previous findings in this population, suggesting an inverse relationship between cholesterol and short-term mortality (26). Indeed, total cholesterol has been reported by others to be inversely associated with the onset of specific diseases and adverse outcomes in the short term. Previous studies have shown a graded negative relationship between total serum cholesterol and risk of nosocomial infections, and in-hospital mortality related to infectious disease has been associated with low cholesterol levels (34,35). Elevated cholesterol concentrations were associated with improved short-term health outcomes after acute stroke of any type (36). In addition, cholesterol levels have been found to be inversely related to mortality after surgery (37). Finally, although total serum cholesterol has been shown to influence coronary heart disease incidence, morbidity, and overall mortality in the long run, it does not impact directly on in-hospital clinical outcomes among patients sustaining acute myocardial infarction (38).

Alternatively, despite the fact that analyses were adjusted for nutritional parameters such as BMI and albumin level, we can not exclude that elevated cholesterol may simply represent an indicator of good nutritional status. In line with this hypothesis, previous observations have shown a direct association between nutritional status parameters and recovery from ADL disability among older adults living in the community (23,24), and several studies of elderly hospitalized patients have identified strong correlations between specific clinical markers of nutritional status (in particular serum proteins, weight loss, and indices of body composition) and the risk of subsequent in-hospital adverse events (39–41).

Finally, despite the fact that we adjusted our analyses for ESR we can not exclude that findings of the study may be explained by the known association between inflammation and cholesterol levels. Indeed, markers of inflammation that were found to be associated with low levels of total cholesterol are associated with disability and poor physical performance among older adults (42,43). In addition, recent studies suggested that cholesterol and its metabolites may be involved in regulation of interleukin-6 signaling, a process known to play a central role in infection, trauma, and regulation of host defense and inflammation, and implicated in the pathogenesis of a number of chronic diseases including ischemic heart disease, rheumatoid arthritis, chronic obstructive pulmonary disease, cancer, and hepatic cirrhosis, which may ultimately lead to disability (44,45).

In the present study, we found no difference in recovery rates between the borderline high (200–240 mg/dL) group and the high (>240 mg/dL) group, suggesting that there is a threshold effect, and that any further increase beyond the borderline high category did not increase or reduce the rate of disability recovery. This finding may be surprising in consideration of the associations between high cholesterol and cardiovascular risk seen in multiple well-conducted studies (27). This difference may be related to the particular characteristics of our study sample. Indeed, the present study includes very old and frail participants, admitted to acute care units because of an acute health condition. Interestingly, studies of very old cohorts did not find any association between high serum cholesterol and all-cause mortality, coronary heart disease mortality, or hospitalization for myocardial infarction or unstable angina (1,4,6). In addition, some studies suggested that high serum cholesterol may be associated with improvement in health outcomes, including all-cause mortality and mortality from cancer and infection (2,3).

The positive association between cholesterol and recovery from ADL disability seems to be in contrast with a previous study showing a beneficial effect of statin use on physical performance in older adults living in the community (46). Extrapolation of findings of the present study could lead to speculation that chronic cholesterol elevation may confer long-term survival to older adults, in which case the utility of cholesterol-lowering therapy in elderly persons, or the benefits of aggressive cholesterol-lowering strategies, could be questioned (47). However, growing evidence suggests that statins may elicit their positive effect not only by lowering cholesterol, but also through a reduction in inflammation (48,49). Results from the Heart Protection Study indicate that statins provide benefit regardless of age, gender, or baseline cholesterol levels (50). In this context, in the population of the present study, use of lipid lowering drugs was associated with a higher rate of recovery from disability.

The rate of use of lipid-lowering drugs in this study is very low, for several possible reasons. First, clear evidence regarding benefits of statin use in older adults became available only recently, after the study was ended (50). Second, participants in the study presented with complex and severe medical conditions requiring hospitalization, and physicians may have set for them clinical priorities different than lower cholesterol levels. Third, patients in the study were already receiving complex drug regimens; therefore, prescribing additional medications may have increased the risk of unwanted drug interactions and the potential for an adverse event.

The present study has several limitations. Although we adjusted all analyses for comorbidity and several indicators of nutritional status and poor health status, it is possible that low cholesterol is simply an indicator of poor health status (8), and that its inverse association with ADL recovery is due to residual confounding and lack of adjustment for factors not measured in the study, such as measures of disease severity. From this point of view, we can not exclude that our results may reflect the fact that, in some patients, reduced total cholesterol may occur secondary to a long-term severely disabling illness, leading to a lower recovery rate in this population. We did not collect data on functional status before hospital admission, which may represent an important confounder because newly disabled older adults recover ADL function at a higher rate that do persons with persistent disability (25). In addition, our results may reflect the fact that, in some patients, reduced total cholesterol may occur secondary to a long-term severely disabling illness or to acute severe illness, leading to a lower recovery rate in this population. Finally, mean length of hospital stay in our population is longer compared with that observed in the United States. Therefore, based on these latter limitations, results of this study can not be generalized to persons living in the community or in other settings.

Conclusion
We report that, among hospitalized disabled older adults, elevated levels of cholesterol are associated with increased rate of recovery from ADL disability. These findings, in conjunction with those from previous reports, suggest that a total cholesterol level ≥200 mg/dL may be desirable in older and disabled adults. Further studies assessing the role of cholesterol in frail elderly persons are warranted.


   Acknowledgments
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The GIFA study was partially supported by a grant from the National Research Council (n. 94000402) and by Neopharmed.

Dr. Onder had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.


   Footnotes
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Decision Editor: Luigi Ferrucci, MD, PhD

Received August 11, 2005

Accepted January 3, 2006


   References
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F. Landi, A. Russo, M. Cesari, M. Pahor, R. Bernabei, and G. Onder
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