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Archives of cardiovascular diseases
Volume 106, n° 4
pages 188-195 (avril 2013)
Doi : 10.1016/j.acvd.2012.12.006
Received : 1 August 2012 ;  accepted : 21 December 2012
Cognitive impairment and malnutrition, predictors of all-cause mortality in hospitalized elderly subjects with cardiovascular disease
Les troubles cognitifs et la malnutrition sont prédictifs de la mortalité chez les patients âgés hospitalisés ayant des maladies cardiovasculaires

Karim Farid a, b, Yi Zhang c, Delphine Bachelier c, Pascaline Gilson c, Antonio Teixeira d, Michel E. Safar c, Jacques Blacher a, b, c, e,
a UMR U557 Inserm, U1125 Inra, CNAM, université Paris 13, CRNH Île-de-France, Bobigny, France 
b Hôpital Hôtel-Dieu de Paris, AP–HP, Paris, France 
c Centre de diagnostic et de thérapeutique, hôpital Hôtel-Dieu de Paris, AP–HP, 1, place du Parvis-Notre-Dame, 75004 Paris, France 
d Service de gériatrie, hôpital Lariboisière-Fernand Widal, AP–HP, Paris, France 
e Université Paris Descartes, Paris, France 

Corresponding author. Centre de diagnostic et de thérapeutique, hôpital Hôtel-Dieu de Paris, AP–HP, 1, place du Parvis-Notre-Dame, 75004 Paris, France. Fax: +33 1 42 34 83 13.

In the elderly, cognitive impairment is associated with loss of independence and may be predictive of mortality.


Our aim was to determine if cognitive impairment correlated to poor prognosis in an elderly (>70 years) hospitalized population with cardiovascular diseases. Our other goal was to explore other factors that might influence mortality risk. Better understanding of these factors should help practitioners select tools to assess these patients and prevent the occurrence of adverse outcomes.


During 4 years of follow-up, medical events and all-cause mortality were reported in 331 patients aged above 70 years, as well as clinical and biological variables and Mini Mental State Examination scores.


Patients with cognitive impairment were older and had a lower body mass index than patients without cognitive impairment (P =0.023). When all factors were forced into the Cox model, cognitive impairment remained an independent predictor of mortality (P <0.001). High plasma glucose, low body mass index and low plasma albumin were associated with overall mortality, independent of cognitive impairment.


In elderly inpatients aged above 70 years with cardiovascular diseases, cognitive impairment and malnutrition are associated, and both are predictors of all-cause mortality. Early nutrition programmes may help to delay mortality, as well as screening the impairment of neuropsychological functioning using the total Mini Mental State Examination score.

The full text of this article is available in PDF format.

Chez les patients âgés, les troubles cognitifs sont accompagnés d’une perte d’indépendance qui pourrait conduire à la mortalité.


L’objectif de cette étude était de déterminer, de façon globale, si les troubles cognitifs sont corrélés à un pronostic plus mauvais chez les sujets âgés (>70ans) hospitalisés, ayant des maladies cardiovasculaires. L’autre objectif était d’explorer les différents facteurs qui pourraient modifier le risque de mortalité. Une meilleure compréhension de ces facteurs pourrait aider les praticiens dans leurs pratiques de prévention.


Pendant quatreans de suivi, les événements intercurrents et les causes de mortalité ont été rapportés chez 331 patients âgés plus de 70ans.


Les analyses statistiques ont montré que les troubles cognitifs représentent un facteur de risque indépendant de la mortalité. Les patients présentant des troubles cognitifs étaient les plus âgés, avaient un index de masse corporelle plus bas que les autres (p =0,023). Quand les autres facteurs de risque étaient introduits dans le modèle statistique, les troubles cognitifs demeuraient un facteur de risque indépendant prédictif de la mortalité (p <0,001). L’hyperglycémie, le faible IMC et l’hypoalbuminémie étaient significativement associés à la mortalité indépendamment des troubles cognitifs.


Chez les sujets âgés (>70ans) hospitalisés ayant des maladies cardiovasculaires, les troubles cognitifs et la dénutrition sont associés et tous les deux sont prédictifs de la mortalité. Des programmes de nutrition adaptés pourraient contribuer à un meilleur pronostic.

The full text of this article is available in PDF format.

Keywords : Cognitive impairment, MMSE, Mortality, Cardiovascular risk factors, Elderly

Mots clés : Troubles cognitifs, MMSE, Mortalité, Facteurs de risques cardiovasculaire, Vieillissement, IMC

Abbreviations : CI, CVD, BMI, HDL, LDL, MMSE, PROTEGER


Impairment of cognitive functions is a common disorder in older people. Cognitive impairment (CI) is associated with decreased memory function and/or other neuropsychological deficits, such as impairment of executive functions, apraxia, agnosia or aphasia. CI represents a major risk factor associated with loss of personal independence and, finally, with the development of dementia, especially Alzheimer’s disease, which is the most common form of neurodegenerative dementia in the elderly [1]. Recent studies on CI, particularly those involving Mini Mental State Examination (MMSE) determinations, have shown the increasing prevalence of dementia with advancing age, affecting around 7% of individuals aged above 65 years and 30% of those aged above 80 years [1, 2, 3]. Thus, patients with CI could exhibit difficulties in completing instrumental activities of daily living, such as managing finances, organizing medications and food preparation [4]. Therefore, a better understanding of the role of multiple factors (as clinical markers) associated with the onset and progression of cognitive decline with advancing age would be useful in the development of new prevention methods. Each year, as an increase in the average life span is observed, the need to perform such studies in the elderly becomes urgent, not only in the ‘young elderly’, but also in those aged above 70 years [5].

Neuropsychological evaluations and mostly novel neuroimaging methodologies suggest that major modifications within the nervous tissue itself (mainly the cerebral white matter) may be at the origin of CI in the elderly [6]. However, there are many arguments suggesting that vascular damage might make a substantial additional contribution [7]. In addition, metabolic and nutritional modifications occur in older people and may interact with vascular factors; both may contribute to overall risk. Finally, increased arterial stiffness may be deleterious for the cardiovascular system, especially in the presence of inflammation or malnutrition [8]. On the other hand, in the elderly population, only type 2 diabetes mellitus remains an important risk factor, as other cardiovascular risk factors do not have the same effect in adults or older people [9].

Although the population profiles of industrialized countries show dramatic increases in the number of elderly people, few studies have focused on CI in very old age [10, 11, 12]. Recently, Strandberg et al. reported that a low MMSE score was predictive of mortality in home-dwelling patients with cardiovascular disease (CVD) aged 75 years or above [13]. However, this study did not explore hospitalized patients, despite them being the most vulnerable and dependent patients and also the most likely to have multiple risk factors for mortality.

Our first working hypothesis was that, in elderly hospitalized subjects aged above 70 years and presenting CVD, CI studied prospectively should also be a good predictor of overall and cardiovascular mortality risk. In addition, we investigated the factors significantly correlated to CI and all-cause mortality, to suggest new therapeutic and prevention methods, particularly in patients presenting CVDs.

Study cohort

Inclusion criteria were as follows: age above 70 years; history of CVD (defined in this study as presence or history of arterial hypertension, coronary heart disease, cerebrovascular disease, history of clinically assessed heart failure or any vascular event of the arteries of the upper or lower limbs, the thoracic or abdominal aorta or the renal arteries); MMSE greater than 15 out of 30 (to make sure the patient could give informed consent to participate in the study), with no severe visual or hearing impairment, absence of fatal disease and life expectancy less than 1 month. Patients with cachexia (body mass index [BMI]<17kg/m2) and/or advanced cancer and/or renal failure (plasma creatinine>250μmol/L) were not included.

From May 2000 to November 2001, 331 consecutive patients (86 men and 245 women) with a mean age±standard deviation of 87±7 years (range: 72–104 years), hospitalized in the geriatric departments of two Île-de-France (Paris suburbs) hospitals (Charles Foix and Emile Roux), were included in the PRonostic cardiovasculaire et Optimisation Thérapeutique En GERiatrie (PROTEGER) study. All patients had CVD; 17% had a history of dyslipidaemia, 21% diabetes, 75% arterial hypertension, 78% coronary heart disease, 22% heart failure, 28% cerebral infarction and 28% peripheral artery disease.

The PROTEGER study was approved by the Committee for the Protection of Human Subjects in Biomedical Research of the Saint-Germain Hospital in Île-de-France. Written informed consent was obtained from all participants after relevant information was given to them and/or to their relatives. Variables that are important for the present analysis are presented here.

Social and clinical characteristics of patients

Information compiled from the questionnaire filled out at inclusion comprised: sex; age; weight; height; personal history of cardiovascular event; presence of diabetes mellitus, dyslipidaemia or arterial hypertension; smoking habits; and previous diseases. The reason for hospitalization and total MMSE score were registered once, at inclusion, in haemodynamically-stabilized conditions. The education level (1 indicates primary school; 2, college degree; 3, bachelor degree; and 4, university degree) was also registered. In some subjects, such information was provided by relatives and/or recorded from the most recent previous hospitalization.

Follow-up procedures

Follow-up started from the baseline examination and lasted until April 2004. Among the 331 participants in the present study, three (1%) were lost to follow-up. Information was obtained from the patients themselves, from their relatives or from general practitioners. Interim telephone and clinic contacts were used to assess all the hospitalizations, outpatient cardiovascular diagnoses and overall mortality. In the case of hospitalization, discharge reports from medical specialists were obtained. Fatal and non-fatal cardiovascular events and all-cause mortality were reported. Follow-up time was defined as the time from the baseline visit to April 2004 for those who survived, to the last contact date for those who were lost to follow-up or to death for the others.

Mini Mental State Examination evaluation

The MMSE, the most commonly administered psychometric screening assessment of cognitive functioning, is a simple and rapid test that may be done by any clinician to evaluate global cognitive functions, especially in primary care [14]. The MMSE has been reported to be a reliable and reproducible method, measuring five areas of cognition labelled as ‘orientation’, ‘registration’, ‘attention and calculation’, ‘recall’, and ‘language’ [14, 15]. A lower MMSE score has been previously reported to predict a higher mortality in subjects with neurological diseases [16] and with CVD [13]. Scores of less than 23–24 points out of 30 have been considered to indicate CI. MMSE scores have been previously reported to be affected by age, education and cultural background, but less by sex [17]. There are no standard cut-offs for the MMSE with regard to education, as prior studies have suggested different cut-offs [18, 19]. In a French population, MMSE was adjusted to educational level and Kalafat et al. defined the pathological cut-off scores as 20–21 in low educational groups and 24 in high educational groups [20]. In this study, MMSE was adjusted to educational level and significant CI was defined as MMSE less than 20 in subjects with primary education (level 1) and less than 24 in subjects with higher education (levels 2, 3 and 4) [19].

Assessment of haemodynamic and biological variables

Haemodynamic measurements were performed in the morning (8.00–10.00a.m.). Brachial blood pressure (BP) was measured after 15 minutes’ rest, using the semiautomatic oscillometric device (Dynamap-Kontron, Paris, France). Aortic pulse wave velocity was determined using the foot-to-foot method in only 283 patients. Venous blood samples were obtained in patients after an overnight fast. Plasma was separated without delay at 4°C in a refrigerated centrifuge and stored at 4°C until analysis. Total cholesterol, triglycerides, high-density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, plasma creatinine, plasma albumin and orosomucoid concentrations were measured as previously described [8].

Statistical analysis

Social, clinical and biological variables, as well as previous cardiovascular events and cardiovascular mortality and all-cause mortality, were compared between subjects with or without CI, using Student’s t test for quantitative variables and the Chi2 test for qualitative variables. Logistic regression models were used to investigate determinants of CI with the stepwise method. The independent association of all-cause mortality with CI was studied by stepwise Cox regression analysis in all subjects and subjects without CI, after adjustment for confounders. Statistical analysis was performed using SAS software, version 9.1 (SAS institute, Cary, NC, USA). A P value<0.05 was considered statistically significant. In Table 1, only significant results have been mentioned in model B.

General characteristics of the population

The population was composed of 331 patients (86 men, 245 women) with a mean age of 87±7 years. All patients had a past history of CVD but the reasons for their hospitalization were as follows: a cardiovascular event (19% of all patients); various physical injuries mostly due to falls (36%); unspecified neuropsychological problems (14%); social reasons (mainly a bridge to a nursing home) (10%); various infections (10%); and other miscellaneous causes (11%). A total of 138 patients (42%) had CI and 191 (58%) had no CI. The mean total MMSE score was 22.2±5.2. After a mean follow-up of 380±196 days (extremes: 50–848 days), 110 subjects (33%) had died.

Table 2 compares the clinical, biological and cardiovascular haemodynamic variables, as well as the medication of CI versus non-CI subjects at the end of follow-up. CI patients were older (P =0.017), although the prevalence of CI with aging was significant in men (n =86; P =0.04) but not in women (n =244; P =0.29). CI patients had a lower BMI (P =0.023) than non-CI patients, an indicator of malnutrition. In contrast with non-CI patients, CI subjects usually lived in an assisted-living community (nursing home) before hospitalization (P =0.050) and tended to have a low mood as they consumed more antidepressive drugs (P =0.092).

All-cause mortality was significantly higher in the CI group compared with in non-CI patients (P <0.001). However, this major finding was not observed for cardiovascular mortality (Figure 1, Figure 2).

Figure 1

Figure 1. 

All-cause mortality (expressed as %) was significantly higher in the cognitive impairment (CI) group compared with in non-CI patients (P <0.001) but a difference was not observed for cardiovascular (CV) mortality.


Figure 2

Figure 2. 

Probability of all-cause survival in subjects with or without cognitive impairment (log-rank: Chi2=16.23; P <0.001).


Cardiovascular risk factors and cognitive impairment

A logistic stepwise regression was conducted, including the covariables age, male sex, location, education rate, residence condition, smoking, antidepressive therapy, BMI, systolic and diastolic BP, heart rate, plasma glucose, total cholesterol, triglycerides, HDL cholesterol and albumin, with the first three variables forced in model A. CI patients had a very high degree of statistical link to low BMI (P =0.009) and high consumption of antidepressive drugs (P =0.017).

Traditional cardiovascular haemodynamic variables, such as carotid systolic BP, carotid diastolic BP, carotid pulse pressure, pulse wave velocity, carotid intima-media thickness and carotid calcification, were not significantly different in the presence or absence of CI (Table 2).

Models predicting all-cause mortality by Cox regression analysis

Cox regression analysis (Table 1) showed that CI was a predictor of mortality, independent of age, sex and residence condition at inclusion (model A). In addition to the three factors in model A, systolic and diastolic BP, heart rate, BMI, smoking, antidepressive therapy, plasma glucose, total cholesterol, HDL cholesterol, triglycerides and albumin were put in model B. The presence of CI remained a major and independent predictor of mortality, even after adjustment for potential confounders in models A and B.

All-cause mortality risk was associated with several independent variables: metabolic factors, with low HDL cholesterol (P =0.011) and high plasma glucose concentrations (P =0.003); and nutritional factors, with low BMI (P =0.004) and low plasma albumin (P <0.001) (Table 1). However, it is worth noting that whereas metabolic factors only directly influence overall mortality, nutritional factors, such as BMI, are also independently associated with CI (Table 2; P <0.023).


This study shows that, in a population of frail hospitalized patients aged above 70 years with a history of CVD, malnutrition (as defined by a low BMI) and cognitive decline (as defined by a low MMSE score) are predictors of overall, but not cardiovascular, mortality. In addition, there are more factors predictive of mortality than cardiovascular factors in this population of very old subjects. These findings were observed even after adjustment for potential confounders, such as age, sex and residence condition, as well as traditional cardiovascular risk factors (Table 2).

The importance of CI in this population can be explained. CI may interfere with the ability of patients with CVD to successfully take up new information and engage in self-care. For example, deficits in memory and attention can impair learning ability and retention of health care information. Deficits in executive functions can interfere with recognizing, interpreting and managing changes in treatment related to CVD [21].

Mini Mental State Examination: limitations and strength

MMSE has been previously reported as a predictor of functional disability in the elderly [22] and as a predictor of mortality in nonagenarian subjects [23].

CI may be undetected without formal screening, suggesting the need of a systematic search with a simple method. The total MMSE score (out of 30) was registered once in this study, at inclusion. Although the cut-off scores of 20 (primary education) and 24 (higher level) are sufficiently accurate to detect patent CI, it is worth noting that total MMSE score is not relevant for screening specific neuropsychological impairments (e.g. apraxia or agnosia) or impairment in executive functions, or for pointing out the nature of the neurological disease (Alzheimer’s disease, vascular dementia, frontotemporal dementia, etc.).

Malnutrition and mortality

It is well known that midlife high BMI is related with a poor outcome. However, this is mainly observed in young cardiovascular patients [12]. In elderly patients, malnutrition (defined as low BMI and low albumin) seems to be associated with a high risk of mortality. Indeed, in elderly patients, BMI is considered a marker of protein stores rather than adiposity itself. Current guidelines suggest a BMI less or equal to 21 as major trigger for nutritional support [24].

Malnutrition may be associated with the previously described reverse metabolic syndrome [9, 25]. The transition to a state of malnutrition, as a sign of the reverse metabolic syndrome, confounds the use of conventional risk factors. As previously described, whereas diabetes remains a major risk factor, the classical role of lipids tends to disappear [9].

Malnutrition was significantly associated with overall mortality and linked to the presence of CI in this study (Table 2). Such results suggest the presence of a significant association between patent CI and malnutrition in frail hospitalized cardiovascular subjects aged above 70 years. Indeed, confusion, low mood and lower functional status as well as hospitalization have been reported to be associated with inadequate nutritional intake and loss of independence [26].

Interestingly, in our population, CI patients had a significantly lower BMI, suggesting that both CI and malnutrition may interact synergistically to the detriment of life expectancy in hospitalized patients. In fact, patients with CI may be unable to cook or may forget to eat or to buy food. Thus, prevention, screening and treatment of malnutrition may deserve higher priority than previously believed in the care of the very old patients. The assessment could be done easily by any healthcare professional, by calculating the BMI.

Regarding prevention, nutritional prevention programmes could be developed and proposed in adulthood, before the risk of cognitive decline arises.

Malnutrition and cognitive impairment: better predictive factors of all-cause mortality than cardiovascular disease

In our study of elderly hospitalized patients, even if nutritional factors and CI could interact synergistically, malnutrition and CI were independent risk factors of all-cause mortality and appeared better predictive factors than CVD (Table 1).

Driver et al. [27], in their prospective cohort study of more than 22,000 male doctors over a 23-year follow-up, reported an increasing rate of major CVD up to the age of 99 years. The authors also reported an increasing cumulative incidence curve for major vascular disease to the age of 100 years. Nevertheless, after adjustment for competing risks for death, they showed a decrease in risk of major CVD in men aged above 80 years. This may be explained by the selective survival of patients who are more resistant to disease. As previously described by Vesin et al., Vischer et al. and Meaume et al. [9, 28, 29], our hospitalized population, who had a history of CVD, was composed mainly of ‘survivors’ owing to the traditional cardiovascular risk factors. This might explain the lack of significant association with CVD, risk factors and mortality.

The geriatric syndrome of frailty, as defined by the consensus supported by the Interventions on Frailty Working Group [30], is recognized to have some predictive value for adverse health outcomes in the elderly population [31]. This geriatric syndrome is considered to be a clinical syndrome characterized by the presence of at least three of the five following components: weight loss; self-reported exhaustion; weakness; slow walking speed; and low physical activity. Avila-Funes et al. [32], in their French three-city study, showed that CI improved the predictive value of this operational clinical definition of frailty. In their study, the risk of death tended to be higher in frail participants with CI than in their non-frail counterparts without CI. In our study, we could hypothesise that patients with malnutrition and CI could also correspond to a frail population, as defined classically and clinically [31]. This point would supply an explanatory basis for the link between malnutrition, CI and mortality, which was significantly observed in our study. Unfortunately, we cannot classify our participants clinically as frail or non-frail patients so we cannot confirm this hypothesis.

Negative findings
Cardiovascular disease and cognitive impairment

It is generally accepted that vascular disorders are positively related to CI, while in this study we considered most of the cardiovascular risk factors, including smoking, obesity, BP, male sex, cholesterol and glucose, but with numerous negative P values. These negative results may suggest that their significant association has been lost, indicating that in the last period of life, vascular diseases or dysfunctions have less influence on CI.

Cardiovascular disease, risk factors and mortality

It is well known that vascular diseases represent a high mortality risk factor. Interestingly, in the present study, neither the traditional cardiovascular risk factors nor the haemodynamic variables indicated in Table 2 were related to mortality in this elderly population. Only hyperglycaemia related to diabetes remained a risk factor.

CVD may be related to reverse metabolic syndrome in the elderly [9, 33]. It is possible that patients with more severe cardiovascular impairments may have died before having the ‘age opportunity’ of entering the study.

Study limitations

This study has several limitations. First, MMSE was the only test used for CI screening. Specific neuropsychological dysfunctions (such as apraxia, agnosia, aphasia or impairment in executive functions) were clinically described by the examiner, but no specific neuropsychological assessment tool (Trail Making Test A and B, Grober and Buschke, verbal fluency, etc.) was used. Furthermore, neither specific neuroimaging examinations nor analysis of cerebrospinal fluid were performed. Thus, the cause of the CI in this population was not determined and CI has been used for classification as a syndrome. In addition, the MMSE was performed only once and, unfortunately, was not repeated. However, it was performed in stabilized conditions. In addition, the same examiner collected the scores. Taken together, all this information reduces the risk of variability regarding the MMSE scores despite the fact that the test was only performed once. In addition, the MMSE was proposed to a relatively small sample but there were a sufficient number of deaths among this subpopulation.

Although the relationship found in this study between CI and increased mortality in older people is well known, few studies have included such very elderly hospitalized participants, all with CVDs.


In our relatively small cohort of very elderly hospitalized patients with cardiovascular conditions, CI (as evaluated by MMSE) and malnutrition (as defined by a low BMI and low plasma albumin) are both predictors of all-cause mortality. These factors have a more important impact on mortality than traditional cardiovascular factors (such as arterial hypertension, high cholesterol concentration or smoking). As both variables are susceptible to modulation by preventive maintenance of mental activities and adequate nutritional support programmes, the ability of their early systematic use to decrease mortality in the very elderly should be tested [24, 26, 34, 35].

Disclosure of interest

The authors declare that they have no conflicts of interest concerning this article.


Author contributions were as follows: K. Farid, writing of the first draft manuscript; Y. Zhang, statistical analysis design, execution, review and critique and manuscript review and critique; D. Bachelier, manuscript review and critique; P. Gilson, manuscript review and critique; A. Teixeira, statistical analysis and manuscript review and critique; M.E. Safar, research project conception, organization and execution and manuscript review and critique; J. Blacher, research project conception, organization and execution and statistical analysis and manuscript review and critique.


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