Artigos

Introduction
Population aging is a global reality, posing a significant challenge to health systems1. This challenge arises from chronic diseases requiring continuous care, medication, and tests. Moreover, there is an increasing demand for health services, accompanied by longer and more frequent hospitalizations among older adults compared to other age groups2.
Sarcopenia and malnutrition are highly prevalent in hospitalized older adults3 and are associated with reduced function, exacerbated underlying diseases, and mortality4,5. Malnutrition results from a lack of nutrient intake or impaired nutrient absorption. This results in body composition changes, such as decreased fat-free mass and reduced physical and mental function6. Sarcopenia is a disease (International Classification of Diseases [ICD]-11M62.84) characterized by decreased muscle mass strength, quality, or quantity, and its severity correlates with the degree of reduced functionality7.
Malnutrition-sarcopenia syndrome (MSS) is characterized by concomitant malnutrition and sarcopenia. This clinically presents a combination of disease burden, inflammation, decreased nutrient intake, and body weight. Further, it includes immune and endocrine disorders; reduced response to oxidative stress; and decreased muscle mass, strength, and physical function8. Given the evidence of a close association between malnutrition and sarcopenia8–10, it is useful to conduct an integrated assessment of nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk in hospitalized older adults and the association with one-year mortality.
In Brazil, there is a lack of studies reporting the prevalence of MSS risk in the older population, and studies investigating nutritional risk and/or malnutrition and sarcopenia risk in hospitalized older adults are scarce and of low-to-moderate quality11–17.
Therefore, understanding the prevalence of nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk at admission in hospitalized older adults can improve clinical monitoring. Furthermore, it can accelerate treatment, effectively enhancing health services for this group.
Our hypothesis is that the prevalence of nutritional risk and the risk of sarcopenia, alone and together, is high in hospitalized older adults and is associated with a higher risk of mortality, and that validated screening questionnaires can be adopted as quick and low-cost resources for early identification and the adoption of appropriate measures.
This study aimed to assess the prevalence of nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk in hospitalized older individuals. Furthermore, it sought to explore the association between these clinical conditions and one-year mortality.

Materials and Methods
This is a retrospective cohort study using malnutrition and sarcopenia screening. Data were collected within 72 h of hospital admission at the Hospital da Previdência do Estado de Minas Gerais (HGIP/IPSEMG), Belo Horizonte, MG, Brazil, from July 2019 to March 2020. This hospital, a public state institution with 350 active beds, provides medium- and high-complexity urgent care and emergency services, surgery, and hospitalization in 40 specialty areas.
The Research Ethics Committee of the Hospital da Previdência do Estado de Minas Gerais (HGIP/IPSEMG) approved the study (opinion no. 5,099,818 and certificate of submission for ethical appraisal no. 50773521.3.0000.5136). This was based on the ethical and scientific principles proposed in resolution 466/2012 of the Brazilian Health Council, and all participants signed an informed consent form. A total of 2425 participants were included using non-probabilistic convenience sampling.
Individuals aged 60 years or older, of both sexes, admitted to various hospital wards, who had undergone screening for malnutrition with the Mini Nutritional Assessment short-form (MNA®-SF) protocol18 and for sarcopenia with the Sluggishness, Assistance in walking, Rising from a chair, Climbing stairs, Falls (SARC-F) questionnaire19 were included in the study. Patients who were younger than 60 years old, admitted to intensive care units or emergency medical services, or did not undergo both screenings as well as individuals who were unable to provide the necessary information for the study were excluded.

Sample Description Variables
The sample was described using the independent variables of age, sex, length of hospital stay, number and classification of medications used, and number and classification of diseases recorded. The diseases were classified according to the ICD-1120, and the medications were classified according to the Brazilian List of Essential Medications (RENAME)21.

Exposure Variables
The variables of nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk were assessed using the MNA®-SF18 (nutritional risk = 8–11 points; malnutrition risk ? 7 points) and the SARC-F19 (sarcopenia risk ? 4 points). MSS risk was defined as the concomitant presence of nutritional risk and/or malnutrition by the MNA®-SF and sarcopenia risk by the SARC-F.
The MNA®-SF is the nutritional screening instrument recommended by the European Society of Parenteral and Enteral Nutrition5 and the European Working Group on Sarcopenia in Older Adults7 and has high sensitivity and reasonable specificity22. The SARC-F is the sarcopenia screening instrument recommended by the Sarcopenia: Revised European Consensus, the Asian Working Group for Sarcopenia, the International Conference on Sarcopenia and Frailty Research Guidelines, and the Society on Sarcopenia, Cachexia and Wasting Disorders and presents high specificity and low–moderate sensitivity23.

Outcome Variable
The outcome variable was one-year mortality from the first day of hospitalization. Death-related data were obtained from the Death Register for beneficiaries of the institutional system and from the Brazilian Register of Deceased Persons at www.falecidosnobrasil.org.br24.

Study Variable Assessment Procedures
Routine admission screening tests were administered by the nutritionist coordinating the hospital service and by a team of previously trained nutrition students and was subsequently verified and signed by activity coordinator. The data were collected from medical records by three specialists in gerontology—a nutritionist, a geriatrician, and a physiotherapist—previously trained using a manual specifically prepared for the study.
Excel software version 2010 was used for data tabulation with an independent double-entry process, followed by automatic database verification of variable response consistency using the “validate double entry” tool of the XL Comparator software25. The principal investigator and the geriatrician generated the final database after error correction.

Statistical Analysis
The sample was descriptively analyzed to obtain central tendency and dispersion measures for quantitative variables and absolute (n) and relative (%) frequency measures for categorical variables. According to Shapiro-Wilk test, there was not a normal distribution, so they were described as median and interquartile range (IQR).
Kaplan–Meier curves were used for survival analysis, and the log-rank test analyzed the model’s sensitivity. A curve was created for the three independent variables: nutritional risk or malnutrition, sarcopenia risk, and MSS risk. The Cox regression model was used to assess the proportionality of risks over the observation time. Results were described as hazard ratio (HR) and 95% confidence interval (CI).
Logistic regression analyses included three independent models as independent predictors of mortality outcomes: one for sarcopenia risk (SARC-F results; no risk and risk), one for malnutrition (MNA®-SF results; normal nutritional status, nutritional risk, and malnutrition), and one for MSS (nutritional risk or malnutrition associated with sarcopenia risk). The models were controlled, first of all, for sex, age, length of hospital stay, number of comorbidities, and number of medications used. But, in the final adjusted model, just age and number of comorbidities were confounders. A log-rank with p < 0.05 indicated a difference between curves. The R Project statistical software version 4.1.0 was used for all analyses26.
All the models were adjusted and assumed proportional hazards, based on residual analysis of Cox regression models using the Laverage test.

Results
A total of 2425 older adults were assessed, mostly women (56.6%), median aged 74 years (IQR 67 – 81). Table 1 presents the clinical and demographic characteristics of the sample. Participants presented a median of 4 (IQR 2 - 5) diseases, used 10 (IQR 7 - 13) medications, and had a mean length of hospital stay of 9 (IQR 5 - 18) days.

Tab. 1

According to the MNA®-SF, most of the group was at nutritional risk (48.2%), and 33.9% were classified as malnourished during the screening. Only 17.9% of the older adults were considered to have a normal nutritional status. The SARC-F showed that 40% of the older adults showed signs of sarcopenia, and the concomitant presence of nutritional risk and/or malnutrition risk and sarcopenia risk was observed in 39.1% of the older adults assessed (Figure 1).

Fig. 1

A total of 323 patients (13.3%) died over the one-year follow-up. Considering mortality, Table 2 shows the percentual of death into each group, considering nutrition, sarcopenia, and MSS.

Tab. 2

Figure 2A–C displays Kaplan–Meier curves illustrating the association between nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk with a greater probability of one-year mortality. Participants with nutritional risk and malnourishment presented a lower one-year survival probability than participants with normal nutritional status (Figure 2A). Older adults at risk for sarcopenia were also less likely to survive (Figure 2B). Participants at risk for MSS were less likely to survive than those without MSS (Figure 2C). All curves presented a log-rank with p < 0.001.

Figure 2. Kaplan-Meier survival curve of hospitalized elderly according to the presence of nutritional risk/malnutrition; risk of sarcopenia and risk of malnutrition-sarcopenia syndrome - Belo Horizonte, MG, 2023.

Fig. 2

Cox multivariate regression analysis (Table 3) showed that the statistically significant variables for mortality outcome were malnutrition (HR 2.17; 95%CI 1.30–3.61; p = 0.003) and MSS risk (HR 1.20; 95%CI 1.10, 1.31; p < 0.001), controlled by age and number of comorbidities. The other variables were excluded in the final model.

Tab. 3

Discussion
This is the first Brazilian study on the prevalence of nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk in hospitalized older adults and the association of these clinical conditions with mortality. A high prevalence of these conditions was observed. Malnutrition and MSS risk were associated with the end point of one-year mortality.
The prevalence of nutritional risk (48.2%) and malnutrition (33.9%) was higher than that reported in other Brazilian studies using the MNA®-SF to analyze hospitalized older adults11–15. In particular, despite using the same criteria to identify nutritional risk or malnutrition, there were insufficient samples. However, our results corroborate international studies with the same objectives and methods27–29. A systematic review and meta-analysis with hospitalized older adults in Europe showed prevalence rates of nutritional risk and malnutrition similar to those reported in the present study of 53% and 28%, respectively 30.
Although there is no standardization among studies on sarcopenia risk, our results (sarcopenia risk of 40% by the SARC-F) align with other Brazilian studies, which reported prevalence rates ranging between 21.8–64.6%16,17. It is important to note that data on the prevalence of sarcopenia risk in hospitalized older patients vary according to the diagnostic method used, including operational definitions, instruments, and cutoff points31.
The present study showed a high prevalence of MSS risk (39.1%). We found no other studies on MSS risk in hospitalized older adults in Brazil to compare results. Nevertheless, this study corroborates a systematic review and meta-analysis including seven studies and 2506 hospitalized older adults in other countries. Specifically, it reported the concomitant presence of sarcopenia and nutritional risk or malnutrition in 41.6% of the sample3. The results of our study on the prevalence of MSS among Brazilian participants are worrisome since Brazil is a developing country with low socioeconomic conditions, prevalent social inequities, and a rapidly increasing older population.
Nutritional risk or malnutrition, sarcopenia risk, and MSS risk reduced one-year survival probability. Cox multivariate regression analysis showed that malnutrition risk and MSS risk were statistically significant for mortality outcome.
Malnutrition (HR 2.17; CI 95% 1.30–3.61) was statistically significantly associated with one-year mortality outcome. Some studies showed that hospitalized older adults with malnutrition have a higher mortality rate32–35. Factors worsening the nutritional status during hospitalization include extended hospital stay, neglected nutritional needs (fasting for diagnostic procedures), dissatisfaction with meals, and disease- or treatment-related loss of appetite 36–38.
Sarcopenia risk did not increase one-year mortality, but older adults at risk for sarcopenia had a lower probability of survival over the same period. However, malnutrition affects the positive score of the specific criteria used to identify sarcopenia by the SARC-F. Thus, the adjusted Cox model may have shown this risk only in malnourished participants.
The literature reports a strong association between mortality and diagnosed sarcopenia (10 XU), but we highlight the difference between sarcopenia risk and diagnosed sarcopenia.
The European Consensus on Sarcopenia7 proposes the assessment of muscle strength (MS) in the presence of risk identified by the screening process, by means of handgrip strength or the sit-to-stand tests, followed by accurate tests in the presence of reduced MS (“probable sarcopenia”), to measure quantity and/or quality in order to confirm the diagnosis.
These include dual-energy X-ray absorptiometry (DXA), bioelectrical impedance analysis (BIA), computed tomography (CT), and magnetic resonance imaging (MRI)7, which are not applicable in most Brazilian hospitals due to several factors including validity (cut-off points, different methods, predictive equations), viability (availability, equipment and personnel costs, structure, portability, safety (radiation) and practicality39,40. In this context, it is recommended to assess the causes and initiate intervention in clinical practice in the presence of reduced FM7.
Data on sarcopenia mortality and risk are limited, especially in hospitalized older adults. We used the SARC-F because it is a standardized screening tool in the institution studied and because the calf circumference of the participants was not measured to calculate the SARC-Calf, which significantly improves the screening performance of the syndrome41.
Our study demonstrated that the group at risk for MSS had a higher one-year mortality risk (HR 1.20; CI 95% 1.10–1.31; p < 0.001). The relationship between mortality and MSS in hospitalized older adults was previously reported in other countries33,42, reinforcing the need for concomitant risk assessment for malnutrition and sarcopenia.
The main characteristics of the studied group are in line with the Brazilian reality: predominance of women43, higher rate of circulatory diseases44,45, and concomitant use of multiple medications [46]. Unlike the results of other studies47–50, the length of hospital stay (15.3 ± 21.4 days) for the sample was significantly higher than the mean for the Brazilian older population (6.5 days) 51. This might be attributed not only to factors such as age, sex, and clinical conditions but also to the high complexity of the institution analyzed. It provides resources for longer therapeutic and propaedeutic plans for the diseases presented.
The results of this study corroborate international guidelines that advocate for nutritional and sarcopenia screening upon admission5–7,52 for older adults. This approach is deemed effective and cost-efficient, facilitating the implementation of more effective preventive interventions and treatments. Malnutrition and sarcopenia have been sufficiently associated with worse prognoses, reduced quality of life, increased use of medical resources, prolonged hospital stay, and increased mortality3,4,10,33–36 to justify a systematic screening process.
Looking ahead, implementing this practice will involve not only making the nutritional screening protocols—established nearly two decades ago by the Ministry of Health for Brazilian public hospitals within the Unified Health System53—mandatory for all private and philanthropic hospitals but also adding sarcopenia risk assessments based on the scientific evidence previously reviewed.
Furthermore, demographic and epidemiological data show limited professional, financial, and technological resources for routine care in Brazil and other countries. This requires reviewing the current healthcare model and identifying specific prognostic indicators for this population specific through the early identification of nutritional risk or malnutrition, sarcopenia risk, and MSS risk by validated, low-cost, and easy-to-use protocols to ensure immediate rehabilitation. Finally, procedures based on service strategies suggest prioritizing nutritional screening when conducting both screenings is not feasible54. Particularly, conducting sarcopenia investigation is recommended only when signs of muscle loss and/or weakness are evident during the malnutrition assessment.
This study has some limitations and strengths. We conducted extensive recruitment of participants, and, although the sample is representative of the issues studied in a public hospital, it does not allow for the extrapolation of the results to other realities. Additionally, the diagnosis of sarcopenia was not performed using CT e RMI7, which are considered the gold standard. Future studies should address these limitations to provide more robust data on this critical topic. The strengths of this study include being a cohort study with a consistent sample.

Conclusions
This first Brazilian study on the prevalence of nutritional risk and/or malnutrition, sarcopenia risk, and MSS risk in hospitalized older adults and their association with mortality showed a high prevalence of these disorders with malnutrition and MSS risk increasing the risk of mortality. In daily health care, the concomitant risk assessment for malnutrition and sarcopenia is a starting point for effectively implementing appropriate approaches in hospital settings.

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