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Preserving muscle is not only crucial for maintaining proper physical movement, but also for its many metabolic and homeostatic roles. Low muscle mass has been shown to adversely affect health outcomes in a variety of disease states (eg, chronic obstructive pulmonary disease, cancer, cardiovascular disease) and leads to an increased risk for readmission and mortality in hospitalized patients. Low muscle mass is now included in the most recent diagnostic criteria for malnutrition. Current management strategies for malnutrition may not prioritize the maintenance and restoration of muscle mass. This likely reflects the challenge of identifying and measuring this body composition compartment in clinical practice and the lack of awareness by health care professionals of the importance that muscle plays in patient health outcomes. As such, we provide a review of current approaches and make recommendations for managing low muscle mass and preventing muscle loss in clinical practice. Recommendations to assist the clinician in the optimal management of patients at risk of low muscle mass include the following: (1) place muscle mass at the core of nutritional assessment and management strategies; (2) identify and assess low muscle mass; (3) develop a management pathway for patients at risk of low muscle mass; (4) optimize nutrition to focus on muscle mass gain versus weight gain alone; and (5) promote exercise and/or rehabilitation therapy to help maintain and build muscle mass. The need to raise awareness of the importance of screening and managing ‘at risk’ patients so it becomes routine is imperative for change to occur. Health systems need to drive clinicians to treat patients with this focused approach, and the economic benefits need to be communicated to payers. Lastly, further focused research in the area of managing patients with low muscle mass is warranted.
of patients are malnourished on hospital admission; many others develop malnutrition during hospitalization. Malnutrition and its consequences place an economic burden on the health care system. Health economic studies have estimated the direct medical costs at more than €31 billion in Europe,
Malnutrition is frequently identified and associated with low body weight and, therefore, management strategies focus on generalized weight gain or maintenance through a higher energy intake. However, more accurately, malnutrition leads to an altered body composition with reduced fat and fat-free body cell mass, leading to diminished physical and mental function and impaired clinical outcome from disease.
Furthermore, low muscle mass results in an increased risk of readmission, falls and fractures, longer hospital stays, disability, reduced functional capacity, loss of independence, and higher risk of mortality in hospitalized patients.
This suggests that loss of muscle mass is one of the most critical consequences of malnutrition. Additionally, certain measures of muscle function have been correlated with muscle mass and can be used to identify patients at nutritional risk and to monitor progress (Table 1). In addition to being a consequence of malnutrition, a natural reduction in muscle mass and function occurs with age resulting in diminished quality of life, greater susceptibility to infection, and an increased risk of mortality.
Managing loss of muscle mass and function is a significant challenge for clinicians, and current treatment approaches warrant revision. In this article, we look at the role that low muscle mass has on health outcomes and discuss some of the available tools and techniques to assess this. Additionally, we provide a series of recommendations that aim to provide useful guidance for clinicians to optimally manage patients at risk of declining muscle mass or those who already present with low muscle mass.
The Importance of Muscle as a Metabolic Organ
Besides its role in the structural maintenance of the body, muscle has been recognized as an important metabolically active and homeostatic organ. Muscle mass is vital in helping to maintain an individual's health, quality of life, and longevity.
Maintenance and restoration of muscle mass with optimal nutritional strategies and, if possible, exercise approaches are crucially important. Both dietary intake (particularly amino acids) and resistance exercise are required to stimulate muscle protein synthesis.
However, these aspects of patient care can often be overlooked, with clinicians’ focus of treatment being the primary disease or condition. Raising awareness of the impact muscle has on health outcomes is an important first step in changing the treatment focus.
Current Malnutrition Screening and Diagnosis Tools Lack a Focus on Muscle Mass
Malnutrition is often unrecognized and undertreated. In a Europe-wide survey of 325 hospitals in 25 countries of more than 21,000 patients, only half reported routine use of nutrition screening tools.
A.S.P.E.N. Board of Directors Consensus statement: Academy of nutrition and Dietetics and American society for Parenteral and enteral nutrition: Characteristics recommended for the identification and documentation of adult malnutrition (undernutrition).
This has several issues, including the failure to recognize that patients with obesity may also be at risk of malnutrition and have low muscle mass. This leads to a focus on increased energy provision for overall weight gain rather than targeting muscle.
To reach global standardization on the identification and endorsement of criteria for the diagnosis of malnutrition, the Global Leadership Initiative on Malnutrition convened to develop a consensus scheme for diagnosing this condition in adults in various clinical settings.
This definition has been endorsed by all major nutrition societies (American Society for Parenteral and Enteral Nutrition, European Society for Parenteral and Enteral Nutrition, Federación Latino Americana de Terapia Nutricional, Nutrición Clínica y Metabolismo, and Parenteral and Enteral Nutrition Society of Asia). The scheme consists of 2 criteria: phenotypic (weight loss, reduced BMI, and reduced muscle mass) and etiologic (reduced food intake/assimilation and disease burden/inflammation). For the diagnosis of malnutrition, the Global Leadership Initiative on Malnutrition recommends using the combination of at least 1 phenotypic criterion and 1 etiologic criterion. The authors of these guidelines indicated that reduced muscle is a strong phenotypic criterion with solid evidence to support its inclusion in the diagnostic process for malnutrition. Thus, the importance of measuring muscle mass during nutrition assessment is acknowledged, and this new criterion will be central to enabling clinicians to center muscle mass within their diagnosis and treatment pathways.
A number of screening tools for identifying patients at risk of malnutrition also exist. However, only one of these include a measure of muscle mass or low mobility—the Mini-Nutritional Assessment (Table 2).
Assessment of Muscle Mass in Clinical Practice
Measurement of muscle mass and function can be used to risk-stratify patients and to monitor response to targeted nutrition interventions. Given the shortcomings of using BMI and weight loss to accurately assess body composition, there are a number of alternative, complementary tools and techniques available that can be used. Each technique varies both in precision and availability (Table 1).
Dual x-ray absorptiometry is frequently regarded as the gold standard for measuring body composition, providing a measure of appendicular lean mass, which is regarded a valid indicator of muscle mass. However, significant barriers including cost, access, and applicability in certain care settings (eg, intensive care unit) limit its use outside of the research and specific clinical settings. Other available techniques for assessing muscle mass, strength, and function are described in Table 1.
Currently, bioelectrical impedance analysis (BIA) is the most widely available and applicable tool to routinely use in clinical practice and can provide a useful guide for estimating muscle mass. One disadvantage of this tool is that the equations used in the estimation of body composition are often not specific to patient cohorts, with the results needing cautious interpretation. Also, a variety of population- or age-specific equations are lacking. Despite this, the use of BIA does seem to be a reasonable choice of technique for tracking longitudinal changes in body composition during treatments and, therefore, could be the method of choice for clinical practice.
Other available techniques for assessing muscle mass and function are described in Table 1.
Despite the availability of a variety of methods to directly or indirectly assess muscle mass (Table 1), it is not routinely measured in clinical practice. As described previously, the reasons for this includes incomplete knowledge and awareness of the condition, how and when to measure, a poor availability of assessment tools, and importantly, a lack of time.
This is further compounded by variations in cost and access to equipment (eg, dual x-ray absorptiometry) and a paucity of regional/population-specific cut-offs to define low muscle mass (eg, in different ethnicities and age groups). Despite these challenges, even in the most resource-limited settings, simple muscle function tests (as described in Table 1) can provide a good surrogate marker, and these tools should be incorporated into clinical practice.
Patients who are experiencing weight loss are at high risk of losing muscle. This includes those who are malnourished or at risk of becoming malnourished, including frail adults; patients with age-associated weight loss; those who are bed-bound or immobile; or patients with diseases or conditions with inflammatory components such as cancer and chronic kidney disease; and those who are critically ill.
Screening patients such as these is crucial for predicting risk and allowing timely interventions to be put in place to stop any further muscle loss. A multidisciplinary approach is ideal but not always feasible in resource-constrained settings, or where there is poor continuity of care as patients are transferred from one clinical setting to another.
A Way Forward—Establishing How Muscle Mass Can Be Maintained and Improved by Nutritional Interventions
Despite the challenges faced, we make the following recommendations to manage and reduce the loss of muscle mass to improve clinical outcomes:
Place muscle mass at the core of nutritional management strategies
Screening and assessment of patients at risk of low muscle mass (eg, older age, inflammation, bed-bound, immobile, in the intensive care unit or those in chronic disease states) is recommended. Furthermore, it would be beneficial for current guidelines to recommend that clinicians include an evaluation of muscle mass and/or function, in addition to other diagnostic criteria, within their nutritional assessment. This will enable optimal management strategies to be put in place, which are focused on maintaining muscle mass.
Improve the management pathway for patients at risk of low muscle mass
Following a specific management pathway to ensure that muscle mass is at the core of the entire nutrition care process, that is, a cycle of screening, assessment, intervention, and monitoring (Figure 1).
Identify and assess low muscle mass for those at risk of malnutrition
Current BMI and weight measurements need to be complemented with practical and precise tools and techniques that will directly assess muscle mass. Estimating muscle mass with BIA may be the most universally practical approach because of its wide availability. However, its limitations still need to be taken into consideration. Using BIA together with muscle function assessment would provide clinicians with readily available ways to better clinically quantify muscle loss. The sensitivity and specificity of these measurements to assess longitudinal changes in different patient cohorts needs to be explored. Where available, dual x-ray absorptiometry scanning is recommended as the gold standard to estimate muscle mass. The use of ultrasound or computed tomography scans may be more applicable and readily available in some clinical settings, especially within oncology and critical care.
Optimize nutrition to focus on muscle gain versus weight gain alone
As a first step, nutritional interventions must provide the patient with adequate energy to hinder muscle catabolism (as protein is used as an energy source).
Protein requirements should then be addressed, as the maintenance or restoration of muscle is dependent on the equilibrium between protein synthesis and degradation. Although protein requirements will vary from person to person, the recommendations are higher for older adults (at least 1.0-1.5 g/kg body weight/d),
Trying to achieve protein targets from diet alone can be challenging in some situations (eg, cancer or critical illness). Supplementing with higher protein feeds can act as an aid to help reach these higher targets. Using high protein oral nutritional supplements (ONS) in the clinical setting has been shown to significantly reduce complications, lower readmissions to hospital and improve handgrip strength and body weight.
Essential amino acids also play a central role in the protein status of a patient. Although many play a role in protein synthesis, branched-chain amino acids and their derivatives are of particular importance for building and maintaining muscle mass.
Of particular note is leucine, the most important regulator of muscle growth, and its metabolite derivative β-hydroxy-β-methylbutyrate (HMB). HMB has been shown to act as a potent stimulator of protein synthesis as well as an inhibitor of protein breakdown.
Therefore, using a high-protein ONS or enteral tube feeding that contains HMB may help in the management of malnutrition and muscle mass loss.
Several other dietary interventions could also help mitigate muscle loss. Vitamin D and omega 3 have been shown to be useful in maintaining and restoring muscle mass and function. Vitamin D supplementation has been shown to improve muscle strength, particularly in those most deficient and within an older age group.
However, individuals who are suffering muscle loss through malnutrition, illness, or aging may have difficulty engaging in physical activities. Adaptations to exercise regimens will need to be made for this population.
Implications for Practice, Policy, And/Or Research
In order for muscle mass to be routinely screened, assessed, and actively managed, there will need to be widespread changes in clinical practice and more focus within the research setting:
Raising awareness—the importance of maintaining/improving muscle mass for patient outcomes needs to be reinforced with both patients and health care professionals
Improved education—more education describing how to assess and manage muscle loss in different health and care settings is needed
New treatment pathways—identifying those at risk of muscle mass loss or with low muscle mass requires different approaches, for example through the involvement of a multidisciplinary team (including medical doctors, registered dietitians, nurses and exercise physiologists), where professionals meet frequently, set up common goals for the patient, and monitor progress together
Better assessment—to identify patients with the correct tools and techniques meant for the right clinical setting
Optimal management—ensure that treatment approaches are optimized to maintain or improve muscle mass
Additional research—determination whether specific nutrition interventions can prevent and/or reverse muscle loss and whether maintenance/gain of muscle is associated with better outcomes in the general patient population as well as in specific conditions
Empowering health professionals to advise on physical activity
The management of patients with malnutrition requires a change to focus on optimizing body composition, specifically muscle mass. A change in our approach starts with the need to raise awareness of the importance of maintaining and building muscle mass to improve health outcomes in our at-risk patients. Screening patients (and thus subsequent treatment) for low muscle needs to become routine, and a variety of assessment tools are already available to help clinicians no matter which clinical setting they practice in. Health systems need to reflect the need to screen at-risk patients and drive clinicians to treat according to this new focus. The economic benefits of this treatment approach need to be more clearly articulated to payers and those in charge of funding decisions. Most importantly for clinicians, placing the maintenance of muscle mass as a focus of our management strategies (including both nutritional support and exercise) will be an effective way to improve the clinical outcomes and quality of life for our patients.
We thank Publicis Resolute who provided medical writing services in the development of this article.
ESPEN guidelines on definitions and terminology of clinical nutrition.
Consensus statement: Academy of nutrition and Dietetics and American society for Parenteral and enteral nutrition: Characteristics recommended for the identification and documentation of adult malnutrition (undernutrition).
This opinion paper was sponsored by Abbott with all authors receiving honorarium for their contributions.
Conflicts of interest: I.A. reports receiving consulting fees from Abbott. Lectures for Abbott, Nutricia and travel grants from Abbott and BBraun. M.B. reports receiving consulting fees from Abbott, Fresenius Kabi and Nestlé Health Science, lectures for Abbott, Fresenius Kabi, Nutricia and Nestlé Health Science, and travel grants from Fresenius Kabi, Nutricia and Abbott. D.E.B. reports receiving advisory board fees, speaker fees and conference attendance support from Nutricia, Nestle Nutrition, BBraun, Baxter Healthcare, Fresenius Kabi, Abbott Nutrition or Cardinal Health. A.J.C.J. reports receiving speakers fees from Abbott Nutrition, Fresenius, Nestlé, Nutricia, Sanofi-Aventis; has been member of advisory boards for Abbott Nutrition, Boehringer Ingelheim Pharma, Nestlé, Pfizer and Regeneron; and has worked on research projects with Novartis, Nutricia, and Regeneron. L.G. reports receiving consulting fees from Abbott, Baxter, Fresenius Kabi and Shire, travel grants from Nestlé Health Science and Abbott and a study grant form Fresenius Kabi . F.L. reports receiving consulting for Incyte, Abbott Nutrition, Nutritcia and academic leader of work package (clinical nutrition) of the SPRINTT project (IMI-JU115621). A.L. reports receiving consulting fees for honoraria for lectures at industry-sponsored events, consulting fees from Abbott, Baxter, BBraun, Fresenius Kabi, Nestlé Health Science, Nutricia, Smartfish and research grant from Fresenius Kabi . K.N. reports receiving consulting fees for advisory board Abbott, unrestricted research grant by Fresenius Kabi and honoria for lectures from Nestle, Fresenius, Nutricia and Abbott. C.M.P. reports receiving travel and honoraria from Abbott Nutrition.