1. Introduction
In older adults, hospitalization due to an acute illness is often associated with increased functional and cognitive decline [
1,
2]. Approximately 35% of older patients are discharged with worse performance in activities of daily living than before being hospitalized [
3]. Consequently, after hospitalization, some older adults are temporarily admitted to an in-patient geriatric rehabilitation ward with the aim of recovering their functional and physical status so that they can return to their homes.
Geriatric rehabilitation, defined by the European Consensus on Geriatric Rehabilitation, provides temporal integral care for older patients following hospitalization [
4]. Although there are large differences between countries regarding the structure and delivery of geriatric rehabilitation, care is usually administered by a multidisciplinary team consisting of at least a physician trained in geriatric rehabilitation, a physiotherapist and a nurse [
4]. Patients admitted to these units include orthogeriatric patients (i.e., patients who have experienced hip fracture, knee replacement or polytraumatism), hospital-deconditioned patients (i.e., patients who have been hospitalized for exacerbation of chronic heart failure, neurologic patients (i.e., patients who have undergone a stroke) and others (i.e., amputees). Rehabilitation usually starts with a comprehensive geriatric assessment with a multidisciplinary approach for the care of older patients [
5,
6]. Furthermore, in-patient rehabilitation services designed for older adults have beneficial effects on functional and cognitive improvement, prevention of institutionalization and reduction of mortality [
7,
8,
9].
Increasing evidence suggests that in older adults, nutritional status is relevant for recovery from an acute illness [
10]. Moreover, poor nutritional status during hospitalization is associated with longer hospitalization and increased mortality rates [
11] and is related to adverse outcomes in a wide variety of acute conditions such as hip fractures [
12] and stroke [
13]. Consequently, early identification of malnutrition in geriatric rehabilitation is especially important since it facilitates nutritional interventions that may help to optimize clinical outcomes. There are different nutritional screening tools directed at older populations, such as nutritional risk screening, mini nutritional assessment (MNA), malnutrition screening test and subjective global assessment [
14,
15]. All of these tools are validated and widely used. However, the European Society for Clinical Nutrition and Metabolism (ESPEN) recommends the MNA, either in its full or short forms, since it also captures physical and mental aspects that frequently affect the nutritional status of the elderly [
16]. The short form of the MNA (MNA-SF) is an easy and rapid nutrition screening tool with good accuracy for assessing malnutrition and risk of malnutrition in older people in different healthcare settings [
17].
The prevalence of malnutrition in older adults is different between healthcare settings and is positively correlated with the level of dependence associated with each care setting as well as the degree of cognitive impairment and number of chronic diseases experienced by the patients [
18]. The lowest malnutrition levels are reported in community-dwelling older adults (<5%), and the highest malnutrition levels are reported in rehabilitation and sub-acute care patients (between 20–36%, depending on the assessment tool used) [
19,
20,
21].
A recent review analyzing nutritional status in geriatric rehabilitation patients reported that malnutrition was negatively associated with functionality, emphasizing the necessity of screening for malnutrition in this population [
22]. Indeed, other studies in these settings have found higher risk of adverse outcomes, such as increased length of stay and mortality, in patients with malnutrition [
23,
24,
25]. Cross-sectional studies in ambulatory geriatric [
26] and home care settings [
27] also associated deficient nutritional status with low physical performance. However, the predictive value of nutritional status on the clinical evolution of geriatric patients throughout the rehabilitation process is poorly understood.
Malnutrition is also related to higher incidence of falls and risk of falling in hospitalized and community-dwelling older adults [
28,
29]. These events can lead to many adverse consequences in this population, such as functional decline, increased morbidity and even death [
30,
31]. However, little is known about relationship between malnutrition and risk of falling in geriatric rehabilitation settings, although low functional and physical performance after hospitalization-deconditioning [
32] may directly increase this risk.
Furthermore, ESPEN classifies malnutrition depending on its etiology. In patients with acute conditions, such as hip fractures, malnutrition is usually injury-related and is characterized by acute pro-inflammatory activity and a fast decline of body energy and nutrient stores. In contrast, chronic disease-related malnutrition, such as chronic heart failure, combines on-going systemic inflammation with chronic weight loss and cachexia [
16]. Consequently, the characteristics of malnutrition may be different depending on the reason for admission to the geriatric rehabilitation ward.
With this background, the first aim of this study was to determine the association between nutritional status at admission and the evolution of functional outcomes and physical performance during an in-patient geriatric rehabilitation process. Secondly, we aimed to analyze the capability of nutritional status at admission to identify patients who are at higher risk of experiencing at least one fall during the period of ward stay. Furthermore, taking into account the different profiles of patients admitted to rehabilitation units, we aimed to clarify whether these associations depend on the reason for the patient’s admission. We hypothesize that worse nutritional status at rehabilitation admission is associated with worse evolution of functional and physical outcomes and with higher risk of being a faller.
4. Discussion
Our findings showed that, in orthogeriatric patients, malnutrition at admission was associated with worse evolution of functional and physical outcomes throughout the rehabilitation process in a geriatric ward. Likewise, poor nutritional status, together with a low MMSE score, was an independent risk factor for being a faller. Nevertheless, in hospital-deconditioned patients, the MNA-SF score at admission did not correlate to the evolution of functional and physical outcomes throughout the rehabilitation process. In this group, a higher SPPB score is an independent risk factor for being a faller.
The prevalence of malnutrition in the present study is higher than that reported in most healthcare settings [
19,
20,
21]. In contrast, other studies that analyzed hospital-deconditioned older patients reported higher levels of malnutrition, similar to the present research [
42,
43]. This difference may be due to the tool used to define malnutrition. Studies with a malnutrition prevalence similar to that in our study used the MNA-SF. However, a lower percentage of malnutrition was found in studies that defined malnutrition using other tools. Notably, the MNA-SF has higher sensitivity but lower specificity than other scales [
44]. This may explain the high prevalence of malnutrition in studies using the MNA-SF since the number of false positives is high, but the number of false negatives is low.
Our results also showed that, in the whole sample, poorer nutritional status at admission was associated with worse evolution of functional and physical outcomes and with increased risk of experiencing a fall throughout the rehabilitation process. However, this association depends on the reason for admission. In orthogeriatric patients, a low MNA-SF score was associated with worse evolution and increased risk of being a faller. In contrast, this association was not observed in hospital-deconditioned patients. This fact may be explained by the different characteristics and malnutrition etiology of hospital-deconditioned and orthogeriatric patients. Hospital-deconditioned patients are usually hospitalized after exacerbation of chronic diseases, and they often have many comorbidities and poor nutritional status, especially patients in advanced disease stages and those who are acutely decompensated [
45,
46]. A high number of comorbidities and poor nutritional status were also identified in the hospital-deconditioned patients analyzed in our study. In these patients, malnutrition could be long-term and related to the severity of the chronic disease with associated cachexia [
47]. In fact, chronic disease patients are known to have chronically decreased muscle mass [
48]. In contrast, orthogeriatric patients, who are usually admitted for a recent acute condition such as a hip fracture, could be more affected by acute changes in nutritional status [
16]. Therefore, we hypothesize that chronic muscle mass loss and severity of symptoms related to chronic disease in hospital-deconditioned patients could modulate the impact of their MNA-SF score on functional and physical recovery. Other scales that measure illness severity, such as the full MNA and/or the assessment of cachexia or chronic inflammatory biomarkers could more accurately predict the clinical evolution of hospital-deconditioned patients in geriatric rehabilitation.
Our findings in orthogeriatric patients are in line with other studies, where nutritional status was associated with functional recovery [
49,
50]. In these studies, follow-up at 3 or 6 months by telephone interview also showed that in patients with poorer nutritional status, functional outcomes remained worse than in those with better status [
49,
50]. To our knowledge, this is the first study to analyze the association between malnutrition at admission and the evolution of physical performance throughout the rehabilitation process in orthogeriatric patients. In a cross-sectional study, Chevalier et al. showed that poorer nutritional status measured by the full MNA was associated with lower gait speed in patients undergoing ambulatory rehabilitation, but reasons for patient admission were not specified [
26]. We observed that orthogeriatric patients with malnutrition at admission had significantly worse SPPB scores throughout the rehabilitation process than those at risk of malnutrition. Poorer physical outcomes in these patients could influence their reduced food intake or assimilation [
16]. These factors could reduce protein availability for muscle and increase muscle catabolism [
51], which could affect lean muscle gain and the positive evolution of physical outcomes throughout the rehabilitation process.
A lower MNA-SF score at admission was also associated with increased risk of being a faller in orthogeriatric patients. Our results also confirm the relationship between nutritional status and falls in orthogeriatric patients in other clinical settings [
28,
29]. A fall represents an adverse outcome that could influence the rehabilitation process with worse functional recovery, increasing the length of stay and reducing the probability of being discharged at home [
52]. Although the tests that usually determine the risk of falling in this population, such as POMA–Tinetti or SPPB, were not included in the multivariable model for predicting patients who fell, the MNA-SF and MMSE scores remained significant in the last equation of the backward regression model. However, the capacity of the MMSE to identify patients at risk of falling agrees with previous studies demonstrating that cognitive impairment increases the risk of falls [
53].
In contrast, we did not find differences in the evolution of any functional or physical outcomes during rehabilitation between malnourished hospital-deconditioned patients and those at risk of malnutrition. These results are in line with other studies, where the direct association between nutritional status and functional outcomes in hospital-deconditioned patients was unclear. Goto et al. [
54] reported that a better MNA-SF score at the start of rehabilitation was only significantly associated with functional recovery in deconditioned patients who were previously more dependent for activities of daily living, while in more independent patients, better nutritional status was not an independent factor for predicting better functional outcomes. In contrast, Katano et al. [
42] reported higher functional gain in patients with worse nutritional status (MNA-SF ≤ 7) than in those with better nutritional status (MNA-SF > 7). In hospital-deconditioned patients, poor nutritional status at admission was not associated with poorer physical recovery. As far as we know, there are no studies that analyze the evolution of physical performance of patients with different nutritional statuses in clinical settings. In a cross-sectional study carried out in deconditioned patients undergoing rehabilitation in a geriatric day hospital, lower nutritional status was not associated with poorer physical performance [
55]. Furthermore, in another cross-sectional study carried out with moderate-to-severe chronic obstructive pulmonary disease (COPD) patients, poorer nutrition did not show an independent association with lower physical performance [
56]. These results suggest that recovery of physical performance in hospital-deconditioned patients could be dependent on other factors not detected by the MNA-SF.
Surprisingly, in deconditioned patients, a higher score on the SPPB test at admission was associated with higher risk of being a faller. Contrary to our findings, lower SPPB has been associated with a higher risk of falls among in-hospital patients and community-dwelling older adults [
57,
58]. However, the SPPB score among hospital-deconditioned fallers in our study was remarkably lower than that in previous studies. We hypothesize that in our study, hospital-deconditioned patients with a higher score on the SPPB might be more independent for displacements and consequently, have a higher chance of experiencing falls than patients with poor physical performance.
An implication of the present study for clinical practice is the usefulness of the MNA-SF nutrition screening tool for prediction of functional and physical outcomes in geriatric rehabilitation patients with acute orthogeriatric conditions. The MNA-SF is recommended by ESPEN for nutrition screening in older adults and is widely used in hospital and rehabilitation settings [
14]. In fact, recently published ESPEN guidelines for clinical nutrition in older persons with malnutrition or at risk of malnutrition encourage nutritional supplementation as well as exercise in older adults with specific diseases following orthopedic surgery, especially for hip fractures [
59], but no specific guidelines are described for hospital-deconditioned patients following rehabilitation.
A strength of this study is that it is the first to assess the relationship between nutritional status and both functional and physical performance outcomes in geriatric rehabilitation patients with different reasons for admission. Additionally, our findings indicate that malnutrition in orthogeriatric patients is a risk-factor for being a faller throughout the rehabilitation process. However, some limitations need to be addressed. First, the MNA-SF is a validated tool for screening of malnutrition, but use of the full MNA might have improved our study´s specificity, particularly in hospital-deconditioned patients. For instance, assessing anthropometric measurements such as mid-arm and calf circumferences and illness severity would further complete the nutritional status assessment. Second, we only assessed the MNA-SF at admission and did not reassess patient nutritional status throughout the process. Therefore, patients who modified their nutritional status during rehabilitation might have different outcomes. Further research is needed to clarify the effects of nutritional status and comprehensive nutritional and exercise interventions in this specific population.