Secondary Logo

Share this article on:

The Crossroads of Aging

An Intersection of Malnutrition, Frailty, and Sarcopenia

Severin, Richard, PT, DPT, CCS; Berner, Patrick M., PT, DPT, RDN; Miller, Kenneth L., PT, DPT, GCS, CEEAA; Mey, Jacob, PhD, RD

Topics in Geriatric Rehabilitation: January/March 2019 - Volume 35 - Issue 1 - p 79–87
doi: 10.1097/TGR.0000000000000218
Pharmacology for the Older Adult: A Primer for the Fine Print

The intersectional relationship between malnutrition, frailty, and sarcopenia in older adults presents unique challenges for health care providers. Malnutrition, specifically, is a leading risk factor for disability, morbidity, and mortality in older adults. Despite improvements in screening procedures, many older adults at risk for malnutrition are not identified, which prevents effective management. Utilizing interdisciplinary approaches toward malnutrition screening is both effective and feasible. Physical therapists can play an important role in both the identification and management of malnutrition in older adults by remaining aware of common nutritional concerns in older adults and performing routine malnutrition screening.

Rehabilitation Science, Department of Physical Therapy, The University of Illinois-Chicago (Dr Severin); Department of Physical Therapy, Baylor University, Waco, Texas (Dr Severin); Fuel Physio, LLC, Taylors, South Carolina (Dr Berner); DPT Program, Touro College, Bay Shore, New York (Dr Miller); Catholic Home Care, Farmingdale, New York (Dr Miller); Integrated Physiology and Molecular Medicine, Pennington Biomedical Research Center, Baton Rouge, Louisiana (Dr Mey); and Inflammation and Immunity, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio (Dr Mey).

Correspondence: Jacob Mey, PhD, RD, Integrated Physiology and Molecular Medicine, Pennington Biomedical Research Center, 6400 Perkins Rd, Baton Rouge, LA 70808 (jacob.mey@pbrc.edu).

The authors confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing, we confirm that we have followed the regulations of our institutions concerning intellectual property.

We further confirm that any aspect of the work covered in this article has been conducted with the ethical approval of all relevant bodies and that such approvals are acknowledged within the article.

In the United States where the population is becoming both older and more medically complex, the management of factors relating to disability, morbidity, and mortality in older adults is of increasing concern.1 Of the many factors associated with disability, morbidity, and mortality risk in older adults, malnutrition is potentially one of the most concerning factors. Malnutrition is a condition defined as a deficiency or excess of energy, protein, and micronutrients resulting in measurable adverse effects on tissue, function, and clinical outcome.2 In older adults, the prevalence of malnutrition and those at risk of developing malnutrition is reported to be approximately 23%,3 with increased prevalence rates in older adults aged 75 to 80 years.3 , 4 Several risk factors for developing malnutrition in older adults have been identified, including chronic illness, medications, economic hardship, social isolation, lower education level, impaired functional status, and symptoms of depression.5 Older adults often possess at least 1 and possibly multiple of these risk factors for malnutrition, which may explain why the prevalence is so high in this population. Many of the risk factors for malnutrition are also interrelated and overlap with other clinical syndromes. For example, frailty, which is defined as the presence of at least 3 of 5 clinical criteria—low grip strength, exhaustion, slowed gait speed, low physical activity, and/or unintentional weight loss,6 is closely related to malnutrition in older adults1 and may be present in approximately 25% of individuals older than 65 years and more than 50% of those older than 85 years.7–10 Both conditions are associated with functional decline, poor quality of life, cognitive impairment, increased health care costs, and increased mortality.11 While malnutrition and frailty are interrelated and may often be concurrently present in older adults,11 , 12 they are distinctly different syndromes. This relationship between frailty and malnutrition may explain why strategies to address either condition can be difficult to implement effectively in older adults.

As described previously, the potential adverse consequences of malnutrition in older adults are numerous. However, the effects of malnutrition on sarcopenia, defined as the loss of skeletal muscle mass and strength,13 are of particular concern in older adults. Beginning in the fourth decade of life, skeletal muscle size, number, and strength decline with increased age alone in a linear fashion14; approximately 50% of muscle mass is lost by the eighth decade of life.15 In addition, the number of skeletal muscle satellite cells, which mediate skeletal muscle repair in response to stress, is also reduced, specifically in type 2 skeletal muscle fibers.16 The presence of malnutrition can potentially exacerbate this age-related decline, leading to impaired functional status, frailty, and sarcopenia (the loss of skeletal muscle).1 , 15 , 17 Sarcopenia may also have additional ramifications throughout the body.18 , 19 Skeletal muscle is highly metabolically active15 and is the primary source of postprandial insulin-stimulated glucose disposal20 and exercise-induced glucose uptake.21 Loss of skeletal muscle mass may predispose older individuals to certain metabolic disorders such as insulin resistance and diabetes.15 , 21 The key regulators of muscle protein synthesis (MPS) are physical activity22 and postprandial plasma essential amino acid availability.22–24 The skeletal muscles of older adults may demonstrate less sensitivity to these anabolic signaling pathways, which is often referred to as “anabolic resistance,”24 especially in the presence of insulin resistance25 and obesity.26 , 27 Therefore, skeletal muscle mass and function, physical activity, and nutritional intake form a complex and interdependent relationship, influencing the health and functional status of older adults.

This intersectional relationship between frailty, sarcopenia, and malnutrition in older adults presents unique challenges for health care providers (Figure). Interdisciplinary collaboration between members of the health care professions is necessary to address the multiple interdependent factors associated with the factors of frailty and malnutrition. A landmark article by Butterworth28 identified that malnutrition was not only frequently encountered in many patients but also negatively affecting patient outcomes, contributing to delayed healing, increased lengths of stay, and elevated hospital costs. Despite decades of effort involving modifications to malnutrition screening procedures, new nutritional supplements, staff and patient education, and a dedication to clinical research, malnutrition in the older adult remains a prevalent issue. Recently, a collaborative effort to address this major issue resulted in the development of the Malnutrition Quality Improvement Initiative, which among many directives, places focus on interprofessional collaboration to address older adult malnutrition. Physical therapists have a unique opportunity to screen and identify patients at risk for malnutrition due to the increased face time and frequent encounters with patients. Utilizing collaborative strategies that improve awareness and routine screening by all members of the health care team has been previously demonstrated to be an effective strategy for identifying patients at risk for malnutrition.29 Recent research also indicates that utilizing collaborative strategies to malnutrition screening is both feasible and results in improved quality of care provided to older adults with malnutrition or at risk for malnutrition.30 This review highlights key principles and strategies to address malnutrition in older adults from the physical therapist perspective.

Figure

Figure

Back to Top | Article Outline

NUTRITIONAL CONCERNS OF OLDER ADULTS

Presently, older adults are living longer and more independent lives and therefore clinicians must consider the nutritional concerns of older adults with long-term health in mind. Of relevance to physical therapists is the maintenance of mobility, muscle function, and muscle mass. Skeletal muscles are fundamental to the locomotion and strength required for completing activities of daily living in older adults.31 The skeletal muscles also play significant roles in various physiological processes throughout the body.18 , 19 , 21 Sarcopenia and the loss of skeletal muscle mass and function have profound clinical significance, as reduced muscle mass and strength predict immobility32 and mortality.33 Although physical therapy interventions are effective at combating loss of skeletal muscle mass and strength,34 the pathogenesis of sarcopenia is multifactorial. This includes not only age-related changes in hormones or inflammation that may require pharmaceutical intervention but also modifiable lifestyle factors such as physical activity and diet.35 Therefore, the combination of physical therapy and nutritional interventions may optimize care in older adults.36 Thus, health care professionals such as physical therapists should understand the primary nutritional components regulating skeletal muscle mass and function in older adults to optimize patient care and achieve desired outcomes, which have proven to be effective at combating malnutrition in other allied health professions.37

Back to Top | Article Outline

PROTEIN

Skeletal muscle is the primary protein reservoir in the body, accounting for more than 33% of total body mass38 and containing more than 40% of total body protein.39 Unlike carbohydrates or fats, which have nontissue storage forms (glycogen and triglycerides, respectively) and are catabolized when exogenous nutrients are not provided, protein must be catabolized from tissue, primarily skeletal muscle tissue. Thus, protein is required for the maintenance of skeletal muscle mass and insufficient protein intake is associated with loss of muscle mass and function, a condition exacerbated with the anabolic resistance of aging. The current dietary guidelines recommend adults consume 0.8 g of protein/kg of body weight. However, because of a variety of physical, mental, social, or economic barriers (Figure), older adults often ingest below the recommended protein intake. Although a major concern is encouraging older adults to consume the recommended protein intake, just as important is whether the current recommendations for adults are appropriate for the older adult.

Recent work has demonstrated that the current recommended dietary allowance (RDA; 0.8 g of protein/kg of body weight) for protein may be inadequate to promote optimal health and muscle function in older adults.40–42 Although long-term intervention trials are lacking, observational studies report improved muscle mass and function with higher protein intake in older adults,43 whereas short-term experimental trials provide strong evidence that increased protein intake results in improved stimulation of skeletal MPS (a primary regulator of skeletal muscle mass).44 The current state of the literature suggests an increase of 50% beyond the RDA (1.2 g of protein/kg of bodyweight) may be required to promote skeletal muscle health in aging.40–42

Recent proceedings from the Protein Summit 2 indicate a need to consider meal-by-meal considerations for protein consumption, beyond just daily requirements, citing 20- to 30-g threshold of leucine-rich protein for optimal signaling of MPS in healthy individuals.45 However, this “meal threshold” of protein and leucine for optimal MPS is reduced with advancing age and defines the anabolic resistance of aging. Current evidence suggests that older adults may require approximately 40 g of leucine-rich protein per meal to reach this MPS stimulatory threshold.46 Given that insufficient protein and leucine intake is well documented, even in homebound older adults,47 ensuring older adults receive proper nutrition counseling is of particular importance. However, protein intake alone is not sufficient to ensure long-term maintenance of skeletal muscle mass.

Back to Top | Article Outline

ENERGY

Just as important as the single macronutrient, protein, is the consumption of enough total energy, or kilocalories each day. The maintenance of body weight balances on the ability to maintain energy intake; an energy deficit promotes body weight loss, and an energy surplus promotes body weight gain. This relationship manifests on the tissue level as well. Therefore, if the goal of a physical therapy intervention is to regain or retain skeletal muscle mass and function, appropriate energy intake is required to optimize the physiological response to physical therapy interventions. Previous studies have demonstrated that lack of appropriate energy intake results in an increased risk of frailty, hospital admissions, and length of stays.48

Back to Top | Article Outline

PRACTICAL IMPLICATION: AWARENESS OF THE NUTRITIONAL PRESCRIPTION

In older adults, physical, mental, or social barriers may exist that limit consumption or access to optimal nutrition including poor dentition, loss of taste or smell, depression, medication interactions, or influences of other chronic diseases. Furthermore, patients recommended for physical therapy services are often at an increased risk of malnutrition49 and may experience lapses of inactivity due to bed rest, exacerbating muscle, and mobility loss.50 Nutritional care for these individuals involves consumption of nutrient-dense and high-calorie foods (such as peanut butter or whole milk), along with recommended nutritional supplements to meet the energy needs of older adults with malnutrition or at risk of malnutrition. Awareness of these nutritional guidelines by physical therapists is important to ensure that consistent messages are provided by all members of the care team.

Back to Top | Article Outline

SUGAR AND ANIMAL PROTEIN

With older adults, addressing recently maligned nutritional concepts is of particular importance. For the general population, recommendations of reducing sugar and animal protein intake are associated with improved health outcomes.51 , 52 However, in older adults, maintaining mobility and muscle mass is of primary concern. Sugar provides a source of palatable calories that may also improve intake of important vitamins, minerals, and protein (an example is a high-calorie milkshake). In this situation, sugar acts as a vehicle for providing optimal nutrition by improving the likelihood of consumption. Similarly, animal protein is high in protein, leucine, and calories per volume of food. In older adults, as previously stated, the volume of food intake can be a limiting factor53 and animal protein provides a nutrient-dense food source, allowing a relatively small meal to breach the “meal threshold” for MPS and support skeletal muscle health and positive energy balance. Physical therapists should communicate these concepts to older adults when discussing nutrition. Maintaining optimal nutritional intake is vital to successful aging.

Back to Top | Article Outline

FOOD-DRUG INTERACTIONS

Older adults may also experience pharmacological interactions, creating additional barriers to meeting recommendations. An older adult's nutritional status may be impacted by food-drug interactions. The interplay of foods and medications may impact both the efficacy of drug therapy and a person's nutritional status, whereas others have suggested that polypharmacy contributes to both frailty and malnutrition.54 Therefore, physical therapists need to understand common food-drug interactions so that referrals may be directed to the registered dietitian for further nutritional evaluation.

The clinical effectiveness of drugs is influenced by absorption, distribution, metabolism, and excretion.55 Absorption is the process of how drugs get into the circulatory system from through the gastrointestinal (GI) tract. Certain foods may increase the bioavailability of a drug, whereas others may interfere with absorption of a medication through the pharmacokinetic actions on the drug.56 When medications have known interactions with drugs, dosing instructions will be provided with regard to when and how to take the medication. The presence of food may change pH, gastric emptying, or alter hepatic blood flow, which may increase or decrease the bioavailability of medications.57 , 58 The bioavailability of certain antibiotics such as penicillin and ciprofloxacin is reduced when taken with foods; yet, other antibiotics such as clarithromycin have increased bioavailability when taken with food.57

Many anticoagulant medications also have significant food-drug interactions, requiring particular consideration.59 Warfarin, which inhibits vitamin K-dependent coagulation factors, has 120 known drug-drug and food-drug interactions, requiring monitoring for variable anticoagulation control.59 Garlic, ginger, caffeine, clove, fish oil, onion, and cranberry may increase the risk of bleeding in patients taking warfarin. Ginseng and green tea have the potential to reduce anticoagulation effects of warfarin.60 Novel anticoagulants such as dabigatran, an oral direct thrombin inhibitor, and oral anti-Factor Xa inhibitors, rivaroxaban, apixaban, and edoxaban, have been developed to address food-drug interaction issues with warfarin treatment. These novel anticoagulants may be taken with or without food, as the bioavailability has not been found to fluctuate based on the presence of food in the GI tract.59

Grapefruit and grapefruit juice has been studied extensively for food-drug interactions due to its inactivation of the CYP3A4 intestinal enzyme and potential prolonged inhibitory effect on intestinal clearance.61 In addition, grapefruit has an inhibitory effect on cellular transporters such as the efflux transporter P-glycoprotein and organic anion-transporting polypeptides mediating influx transport. Many grapefruit-drug interactions are fairly innocuous; however, some are more significant. For example, patients receiving statin therapy should avoid grapefruit juice due to the increased risk of developing rhabdomyolysis and myalgia.61 Grapefruit may also increase the plasma concentration of calcium channel blockers.62

Although this list of food-drug interactions is not exhaustive, the need for physical therapists to be aware of potential food-drug interactions in older patients is clearly demonstrated. These interactions also demonstrate the importance of open communications with other members of the health care team including registered dietitians, pharmacists, and physicians.

Back to Top | Article Outline

DRUG-APPETITE INTERACTION

Appetite is defined as a sensation of hunger that promotes food consumption, and satiation is the feeling of fullness that leads to meal termination and satiety between meals.63 , 64 Appetite is controlled by short- and long-term mechanisms that influence feeding behavior. Short-term mechanisms include sensors in the GI tract that sense the presence or absence of food and food composition such as fat or protein stimulating or inhibiting appetite.63 , 64 Long-term mechanisms rely on the release of various hormones such as ghrelin secreted from the stomach in response to the fasting state that serves to increase appetite. Other long-term mechanisms include the release of peptide YY from the ileum and colon, resulting in suppression of appetite in response to food intake.63 , 64 Cholecystokinin is released from the small intestine in response to the presence of protein and fat to suppress appetite. Insulin is secreted by the pancreas in response to high blood glucose levels to reduce blood glucose levels by increasing uptake into the skeletal muscles and suppressing appetite.63 , 64

Poor appetite contributes to unintentional weight loss, malnutrition, and poor health outcomes including mortality.63 In older adults, appetite decline may be attributed to several factors including physiological effects of aging, psychological functioning, social circumstances, acute illness, chronic disease, or medications.63 As for medications, more than 200 medications have been identified as altering both the taste and smell of food or causing nausea, which may reduce appetite. More than 18 drug classes have been identified as impairing appetite including the following drug classes: antibiotics, cardiac medications, psychotropic medications, statins, and nonsteroidal anti-inflammatory drugs.63 Impaired appetite may have potential ramifications on mobility and the rehabilitation processes.65 Therefore, physical therapists need to understand that older adults may have reduced appetite due to the normal physiological effects of aging and/or potential effects of certain medications. Physical therapists should collaborate with members of the allied health care team such as registered dietitians, pharmacists, and physicians to appropriately manage impaired appetite in older patients.

Back to Top | Article Outline

EFFECTS ON REHABILITATION DUE TO POOR NUTRITIONAL INTAKE

Nutritional intake affects all metabolic processes of the human body and may also influence rehabilitation outcomes. Impaired nutritional intake or malnutrition has been found to negatively impact functional abilities and quality of life.65 Therefore, the impact of nutritional intake is of particular concern in older patients due to the increased prevalence of malnutrition and sarcopenia in this population, which are estimated to be upward of 50.5% and 40%, respectively.36

Poor nutrition is detrimental to older adults through loss of muscle mass and strength. However, optimizing nutrition may play a synergistic role in improving rehabilitation. Nutritional intervention in older adults improves recovery during posthospitalization,40 benefiting outcomes relevant to physical therapy such as handgrip strength66 and fall risk.67 Supporting data specific to combining nutrient intake and rehabilitation in older adults is feasible68 and promising, but limited.36 Until additional research is available to validate the combination of nutrient intake and rehabilitation therapy, implications can be drawn from studies surrounding nutrient intake and exercise training in older adults, as this mimics the functional mobility and muscle performance outcome goals of physical therapy interventions in this population. For example, the combination of nutritional supplementation with aerobic exercise69 or resistance exercise70 in older adults promotes greater improvements in muscle mass and strength than aerobic or resistance exercise alone.71 , 72

Back to Top | Article Outline

PRACTICAL IMPLICATIONS: NUTRITIONAL SCREENING AND REFERRAL

Adequate nutrition promotes beneficial adaptations in older adults, whereas malnutrition exacerbates functional decline. For other innovative approaches to address the intersection of nutrition, frailty, and sarcopenia, the readers are directed to a recent review.73 It is the role of the registered dietitian to identify a patient's nutritional needs, plan and implement nutritional interventions, and monitor the special needs of older adults. However, individuals with malnutrition or at risk for malnutrition are too often missed and not appropriately referred to registered dietitians for medical nutrition therapy. Some studies suggest that less than 10% of malnourished patients are appropriately identified in the hospital setting74 and may be even less identified in other populations such as community-dwelling older adults.74 This lack of identification prevents timely and effective nutritional care.

Therefore, how do other health care professionals, such as physical therapists, determine whether a nutritional problem exists or whether nutritional intervention is needed by a registered dietitian? Identifying older patients at risk for malnutrition can be accomplished by the addition of a simple screening process, performed by any member of the health care team, through the utilization of a standardized nutritional screening tool. It is important to note that nutritional screening by physical therapists is supported by the American Physical Therapy Association's House of Delegate position statement, P06-15-22-17, The Role of the Physical Therapist in Diet and Nutrition, which states that “it is the role of the physical therapist to screen for and provide information on diet and nutritional issues to patients, clients, and the community within the scope of physical therapist practice.”75 Although it is now suggested that identification of malnutrition requires a collaborative approach, physical therapists can play a pivotal role in identifying patients at risk for malnutrition. However, if a patient screens positive for malnutrition or malnutrition risk, a referral to a registered dietitian for further nutritional assessment should be made. In such a case, the patient may require medical nutrition therapy, which cannot be performed by the physical therapist. Importantly, malnutrition screening not only should aid in the identification of older adult patients at risk for malnutrition but should also create an open line of communication between all members of the health care team and develop a streamlined referral process.

Since there is no gold standard for screening malnutrition, the use of a standardized tool may be the best option for screening purposes. Some commonly used tools include the Malnutrition Screening Tool (MST),76 the Malnutrition Universal Screening Tool (MUST),77 and the Mini Nutrition Assessment-Short Form (MNA-SF).78 Each of the tools can be administered in a timely manner and provide greater insight into a patient's risk for malnutrition; these are detailed in the Table. Either of these tools can be easily implemented by a physical therapist to assess the patient's risk of malnutrition. Of note, these screening tools do not assess the overall quality of nutritional intake, as a registered dietitian is required for that purpose.

TABLE

TABLE

Aside from the use of standardized tools, the Academy of Nutrition and Dietetics (AND) and the American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.) have identified 6 characteristics that associate with an increased risk of malnutrition.79 These characteristics include insufficient energy intake, weight loss, loss of muscle mass, loss of subcutaneous fat, localized or generalized fluid accumulation, and diminished functional status as measured by handgrip strength.79 When 2 or more of these characteristics are present, a diagnosis of malnutrition is recommended. Five of these 6 characteristics are easily identifiable by a physical therapist since they are strongly correlated to functional mobility and some of these assessments are components of a routine physical therapy examination. Therefore, the implementation of routine malnutrition screening appears to be feasible for physical therapists.

Within the screening process, the clinician must also identify whether the need for referral to a registered dietitian is warranted, based on the patient's current presentation, medical history, and the screening clinician's scope of practice. An example of this scenario would be a patient who possesses a medical condition that has shown to be strongly correlated with nutritional intake or the presence of complex medication interactions. If referral were to occur, a nutritional assessment would be completed by the registered dietitian to further identify risk and needs for appropriate intervention. In some cases, an immediate referral may not be warranted or available and in that case the treating clinician would offer basic nutritional education as is appropriate per the scope of practice of the physical therapist (which may vary by US states). Nutrition education involves sharing basic nutrition knowledge on healthy eating for older adults, which should be obtained from validated resources. These educational resources should be obtained from validated resources, such as the US Department of Health and Human Services' and the US Department of Agriculture's Dietary Guidelines for Americans80 or the AND's Dietary Guidelines and MyPlate for Seniors.81

Back to Top | Article Outline

NUTRITIONAL EDUCATION VERSUS MEDICAL NUTRITION THERAPY

Medical nutrition therapy is nutrition diagnosis, intervention, and counseling implemented by the registered dietitian and is beyond the scope of the physical therapist.82 Nutritional education is the reinforcement of basic or essential nutritional information and may be provided by a physical therapist or physical therapist assistant. Clinicians must distinguish these concepts and most importantly they must stay within the scope of their practice. However, nutritional education is within the physical therapist's scope and can be implemented by providing generalized nutritional information and helpful tips for healthier food and fluid intake or directing patients to available and validated resources such as those mentioned previously.80 , 81 Outside of direct patient interaction, the clinician can also advocate for federal, state, and local food and nutrition programs and services, especially within the home and community setting.83

Back to Top | Article Outline

SUMMARY

Malnutrition has significant consequences on patient outcomes, especially in older adults. Unfortunately, many older adults who are malnourished go untreated because of gaps in screening for malnutrition and malnutrition risk. Physical therapists can play an important role in the identification and management of malnutrition and malnutrition risk by remaining aware of common concerns in older adults and by performing routine malnutrition screening. Although medical nutrition therapy is performed by registered dietitians, physical therapists can provide basic nutritional education and should do so while acknowledging their scope of practice and their patients' medical and nutritional needs. In addition, the combination of physical therapy and nutritional interventions may provide optimal patient outcomes. Despite variations in scope of practice, all members of the health care team must strive to improve patient care through interprofessional communication and collaboration.

Back to Top | Article Outline

References

1. Agarwal E, Miller M, Yaxley A, Isenring E. Malnutrition in the elderly: a narrative review. Maturitas. 2013;76(4):296–302. doi:10.1016/j.maturitas.2013.07.013.
2. Stratton RJ, Green CJ, Elia M. Scientific criteria for defining malnutrition. In: Disease-Related Malnutrition: An Evidence-Based Approach to Treatment. Wallingford, UK: CABI; 2003.
3. Kaiser MJ, Bauer JM, Rämsch C, et al Frequency of malnutrition in older adults: a multinational perspective using the mini nutritional assessment. J Am Geriatr Soc. 2010;58(9):1734–1738. doi:10.1111/j.1532-5415.2010.03016.x.
4. Ljungqvist O, van Gossum A, Sanz ML, de Man F. The European fight against malnutrition. Clin Nutr. 2010;29(2):149–150. doi:10.1016/j.clnu.2009.10.004.
5. Robb L, Walsh CM, Nel M, Nel A, Odendaal H, van Aardt R. Malnutrition in the elderly residing in long-term care facilities: a cross sectional survey using the Mini Nutritional Assessment (MNA®) screening tool. South African J Clin Nutr. 2017;30(2):34–40. doi:10.1080/16070658.2016.1248062.
6. Xue QL. The frailty syndrome: definition and natural history. Clin Geriatr Med. 2011;27(1):1–15.
7. National Nutrition Monitoring and Related Research Act of 1990. Pub L No. 101-445, 104 Stat 1034, 101st Cong An Act (1990).
8. Clegg A, Young J, Iliffe S, Olde Rikkert MGM, Rockwood K. Frailty in older people. Lancet. 2013;381(9868):752–762. doi:10.1016/S0140-6736(12)62167-9.
9. Rockwood K, Song X, MacKnight C, et al A global clinical measure of fitness and frailty in elderly people. CMAJ. 2005;173(5):489–495. doi:10.1503/cmaj.050051.
10. Hoover M, Rotermann M, Sanmartin C, Bernier J. Validation of an index to estimate the prevalence of frailty among community-dwelling seniors. Heal Rep. 2013;24(9):10–17.
11. Wei K, Nyunt MSZ, Gao Q, Wee SL, Ng TP. Frailty and malnutrition: related and distinct syndrome prevalence and association among community-dwelling older adults: Singapore Longitudinal Ageing Studies. J Am Med Dir Assoc. 2017;18(12):1019–1028. doi:10.1016/j.jamda.2017.06.017.
12. Laur CV, McNicholl T, Valaitis R, Keller HH. Malnutrition or frailty? Overlap and evidence gaps in the diagnosis and treatment of frailty and malnutrition. Appl Physiol Nutr Metab. 2017;42(5):449–458. doi:10.1139/apnm-2016-0652.
13. Studenski SA, Peters KW, Alley DE, et al The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69(5):547–558. doi:10.1093/gerona/glu010.
14. Lexell J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci. 1995;50(Spec No.):11–16. doi:10.1093/gerona/50A.Special_Issue.11.
15. Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol. 2012;24(6):623–627. doi:10.1097/BOR.0b013e328358d59b.
16. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HHCM, van Loon LJC. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. AJP Endocrinol Metab. 2006;292(1):E151–E157. doi:10.1152/ajpendo.00278.2006.
17. Morley JE. Frailty and sarcopenia in elderly. Fam Pract. 2012;29(1):i44–i48. doi:10.1093/fampra/cmr063.
18. Pedersen L, Hojman P. Muscle-to-organ cross talk mediated by myokines. Adipocyte. 2012;1(3):164–167. doi:10.4161/adip.20344.
19. Raschke S, Eckardt K, Bjørklund Holven K, Jensen J, Eckel J. Identification and validation of novel contraction-regulated myokines released from primary human skeletal muscle cells. PLoS One. 2013;8(4):e62008. doi:10.1371/journal.pone.0062008.
20. DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care. 2009;32(suppl 2):S157–S163. doi:10.2337/dc09-S302.
21. Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 2013;93(3):993–1017. doi:10.1152/physrev.00038.2012.
22. Koopman R, Van loon LJ. Aging, exercise, and muscle protein metabolism. J Appl Physiol. 2009;106(6):2040–2048.
23. Bohé J, Low A, Wolfe RR, Rennie MJ. Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J Physiol. 2003;552(1):315–324. doi:10.1113/jphysiol.2003.050674.
24. Cuthbertson D, Smith K, Babraj J, et al Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005;19(3):422–424.
25. Cleasby ME, Jamieson PM, Atherton PJ. Insulin resistance and sarcopenia: mechanistic links between common co-morbidities. J Endocrinol. 2016;229(2):R67–R81. doi:10.1530/JOE-15-0533.
26. Allen DL, Hittel DS, McPherron AC. Expression and function of myostatin in obesity, diabetes, and exercise adaptation. Med Sci Sports Exerc. 2011;43(10):1828–1835. doi:10.1249/MSS.0b013e3182178bb4.
27. Tomlinson DJ, Erskine RM, Morse CI, Winwood K, Onambélé-Pearson G. The impact of obesity on skeletal muscle strength and structure through adolescence to old age. Biogerontology. 2016;17(3):467–483. doi:10.1007/s10522-015-9626-4.
28. Butterworth CE Jr. Editorial: Malnutrition in the hospital. JAMA. 1974;230(6):879.
29. Souza TT, Sturion CJ, Faintuch J. Is the skeleton still in the hospital closet? A review of hospital malnutrition emphasizing health economic aspects. Clin Nutr. 2015;34(6):1088–1092. doi:10.1016/j.clnu.2015.02.008.
30. Silver HJ, Pratt KJ, Bruno M, Lynch J, Mitchell K, McCauley SM. Effectiveness of the Malnutrition Quality Improvement Initiative on practitioner malnutrition knowledge and screening, diagnosis, and timeliness of malnutrition-related care provided to older adults admitted to a tertiary care facility: a pilot study. J Acad Nutr Diet. 2018;118(1):101–109. doi:10.1016/j.jand.2017.08.111.
31. Reid KF, Fielding RA. Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev. 2012;40(1):4–12. doi:10.1097/JES.0b013e31823b5f13.
32. McLean RR, Shardell MD, Alley DE, et al Criteria for clinically relevant weakness and low lean mass and their longitudinal association with incident mobility impairment and mortality: the foundation for the National Institutes of Health (FNIH) sarcopenia project. J Gerontol A Biol Sci Med Sci. 2014;69(5):576–583. doi:10.1093/gerona/glu012.
33. Landi F, Liperoti R, Russo A, et al Association of anorexia with sarcopenia in a community-dwelling elderly population: results from the ilSIRENTE study. Eur J Nutr. 2013;52(3):1261–1268. doi:10.1007/s00394-012-0437-y.
34. Vlietstra L, Hendrickx W, Waters DL. Exercise interventions in healthy older adults with sarcopenia: a systematic review and meta-analysis. Australas J Ageing. 2018;37(3):169–183. doi:10.1111/ajag.12521.
35. Rolland Y, Czerwinski S, Abellan Van Kan GA, et al Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J Nutr Health Aging. 2008;12(7):433–450. doi:10.1007/BF02982704.
36. Wakabayashi H, Sakuma K. Rehabilitation nutrition for sarcopenia with disability: a combination of both rehabilitation and nutrition care management. J Cachexia Sarcopenia Muscle. 2014;5(4):269–277. doi:10.1007/s13539-014-0162-x.
37. Fernández-Barrés S, García-Barco M, Basora J, et al The efficacy of a nutrition education intervention to prevent risk of malnutrition for dependent elderly patients receiving home care: a randomized controlled trial. Int J Nurs Stud. 2017;70:131–141. doi:10.1016/j.ijnurstu.2017.02.020.
38. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D. Total-body skeletal muscle mass: estimation by a new dual-energy x-ray absorptiometry method. Am J Clin Nutr. 2002;76(2):378–383. doi:10.1093/ajcn/76.2.378.
39. Lentner C, ed. Geigy Scientific Tables. Vol 1. 8th ed. West Caldwell, NJ: Ciba-Geigy Corporation; 1981.
40. Deer RR, Volpi E. Protein requirements in critically ill older adults. Nutrients. 2018;10(3). doi:10.3390/nu10030378.
41. Traylor DA, Gorissen SHM, Phillips SM. Perspective: protein requirements and optimal intakes in aging: are we ready to recommend more than the recommended daily allowance? Adv Nutr. 2018;9(3):171–182. doi:10.1093/advances/nmy003.
42. Baum JI, Wolfe RR. The link between dietary protein intake, skeletal muscle function and health in older adults. Healthcare (Basel). 2015;3(3):529–543. doi:10.3390/healthcare3030529.
43. Velázquez Alva MDC, Irigoyen Camacho ME, Delgadillo Velázquez J, Lazarevich I. The relationship between sarcopenia, undernutrition, physical mobility and basic activities of daily living in a group of elderly women of Mexico City. Nutr Hosp. 2013;28(2):514–521. doi:10.3305/nh.2013.28.2.6180.
44. Granic A, Mendonça N, Sayer AA, et al Low protein intake, muscle strength and physical performance in the very old: the Newcastle 85+ Study. Clin Nutr. 2018;37(6 Pt A):2260–2270. doi: 10.1016/j.clnu.2017.11.005
45. Santarpia L, Contaldo F, Pasanisi F. Dietary protein content for an optimal diet: a clinical view. J Cachexia Sarcopenia Muscle. 2017;8(3):345–348. doi:10.1002/jcsm.12176.
46. Paddon-Jones D, Rasmussen BB. Dietary protein recommendations and the prevention of sarcopenia. Curr Opin Clin Nutr Metab Care. 2009;12(1):86–90. doi:10.1097/MCO.0b013e32831cef8b.
47. Dasgupta M, Sharkey JR, Wu G. Inadequate intakes of indispensable amino acids among homebound older adults. J Nutr Elder. 2005;24(3):85–99. doi:10.1300/J052v24n03_07.
48. Roberts SB, Hajduk CL, Howarth NC, Russell R, McCrory MA. Dietary variety predicts low body mass index and inadequate macronutrient and micronutrient intakes in community-dwelling older adults. J Gerontol A BiolSci Med Sci. 2005;60(5):613–621.
49. Souza I, Oliveira Neta RS, Gazzola JM, Souza MC. Elderly with knee osteoarthritis should perform nutritional assessment: integrative literature review. Einstein (Sao Paulo). 2017;15(2):226–232. doi:10.1590/S1679-45082017RW3834.
50. Breen L, Stokes KA, Churchward-Venne TA, et al Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly. J Clin Endocrinol Metab. 2013;98(6):2604–2612. doi:10.1210/jc.2013-1502.
51. Johnson RK, Appel LJ, Brands M, et al Dietary sugars intake and cardiovascular health: a scientific statement from the American Heart Association. Circulation. 2009;120(11):1011–1020. doi:10.1161/CIRCULATIONAHA.109.192627.
52. Sofi F, Cesari F, Abbate R, Gensini GF, Casini A. Adherence to Mediterranean diet and health status: meta-analysis. BMJ. 2008;337:a1344. doi:10.1136/bmj.a1344.
53. Wurtman JJ, Lieberman H, Tsay R, Nader T, Chew B. Calorie and nutrient intakes of elderly and young subjects measured under identical conditions. J Gerontol. 1988;43(6):B174–B180.
54. Wakabayashi H. Rehabilitation pharmacotherapy: a combination of rehabilitation and pharmacotherapy. J Gen Fam Med. 2018;19(2):43–44. doi:10.1002/jgf2.163.
55. Klotz U. Pharmacokinetics and drug metabolism in the elderly. Drug Metab Rev. 2009;41(2):67–76. doi:10.1080/03602530902722679.
56. Gu CH, Li H, Levons J, et al Predicting effect of food on extent of drug absorption based on physicochemical properties. Pharm Res. 2007;24(6):1118–1130. doi:10.1007/s11095-007-9236-1.
57. Adithan C. Food & drug bioavailability. Indian J Med Res. 2005;121(5):631–633.
58. Brewer L, Williams D. Clinically relevant drug-drug and drug-food interactions: underlying mechanisms and regulatory requirements for drug licensing. Pharm Med. 2013;27(1):9–23. doi:10.1007/s40290-013-0008-4.
59. Nutescu E, Chuatrisorn I, Hellenbart E. Drug and dietary interactions of warfarin and novel oral anticoagulants: an update. J Thromb Thrombolysis. 2011;31(3):326–343. doi:10.1007/s11239-011-0561-1.
60. Ge B, Zhang Z, Zuo Z. Updates on the clinical evidenced herb-warfarin interactions. Evid Based Complement Alternat Med. 2014;2014:957362. doi:10.1155/2014/957362.
61. Seden K, Dickinson L, Khoo S, Back D. Grapefruit-drug interactions. Drugs. 2010;70(18):2373–2407. doi:10.2165/11585250-000000000-00000.
62. Mahata PP, Thakur A, Chakraborty S, Bala NN. A review on pharmacist's role in mitigation of food-drug interactions. Res J Pharm Technol. 2015;8(4):423–431. doi:10.5958/0974-360X.2015.00071.2.
63. Pilgrim AL, Robinson SM, Sayer AA, Roberts HC. An overview of appetite decline in older people. Nurs Older People. 2015;27(5):29–35. doi:10.7748/nop.27.5.29.e697.
64. Gasque G. An appetite for understanding appetite. PLoS Biol. 2017;15(5):1–4. doi:10.1371/journal.pbio.2002838.
65. Marshall S, Bauer J, Isenring E. The consequences of malnutrition following discharge from rehabilitation to the community: a systematic review of current evidence in older adults. J Hum Nutr Diet. 2014;27(2):133–141. doi:10.1111/jhn.12167.
66. Price R, Daly F, Pennington CR, McMurdo ME. Nutritional supplementation of very old people at hospital discharge increases muscle strength: a randomised controlled trial. Gerontology. 2005;51(3):179–185. doi:10.1159/000083991.
67. Neelemaat F, Lips P, Bosmans JE, Thijs A, Seidell JC, van Bokhorst-de van der Schueren MA. Short-term oral nutritional intervention with protein and vitamin D decreases falls in malnourished older adults. J Am Geriatr Soc. 2012;60(4):691–699. doi:10.1111/j.1532-5415.2011.03888.x.
68. Deer RR, Goodlett SM, Fisher SR, et al A randomized controlled pilot trial of interventions to improve functional recovery after hospitalization in older adults: feasibility and adherence. J Gerontol A Biol Sci Med Sci. 2018;73(2):187–193. doi:10.1093/gerona/glx111.
69. Markofski MM, Jennings K, Timmerman KL, et al Effect of aerobic exercise training and essential amino acid supplementation for 24 weeks on physical function, body composition and muscle metabolism in healthy, independent older adults: a randomized clinical trial. J Gerontol A Biol Sci Med Sci. 2018. doi:10.1093/gerona/gly109.
70. Nabuco HCG, Tomeleri CM, Sugihara P Junior, et al Effects of whey protein supplementation pre- or post-resistance training on muscle mass, muscular strength, and functional capacity in pre-conditioned older women: a randomized clinical trial. Nutrients. 2018;10(5). doi:10.3390/nu10050563.
71. Martínez-Amat A, Aibar-Almazán A, Fábrega-Cuadros R, et al Exercise alone or combined with dietary supplements for sarcopenic obesity in community-dwelling older people: a systematic review of randomized controlled trials. Maturitas. 2018;110:92–103. doi:10.1016/j.maturitas.2018.02.005.
72. Thomas DK, Quinn MA, Saunders DH, Greig CA. Protein supplementation does not significantly augment the effects of resistance exercise training in older adults: a systematic review. J Am Med Dir Assoc. 2016;17(10):959.e1–959.e9. doi:10.1016/j.jamda.2016.07.002.
73. Cruz-Jentoft AJ, Kiesswetter E, Drey M, Sieber CC. Nutrition, frailty, and sarcopenia. Aging Clin Exp Res. 2017;29(1):43–48. doi:10.1007/s40520-016-0709-0.
74. Weiss AJ, Fingar KR, Barrett ML, et al Characteristics of hospital stays involving malnutrition, 2013. In: Healthcare Cost and Utilization Project (HCUP) Statistical Briefs. Rockville, MD: Agency for Healthcare Research and Quality; 2006. Statistical Brief No. 210. https://www.ncbi.nlm.nih.gov/pubmed/27854406. Accessed May 15, 2018.
75. APTA. Patient care: nutrition and physical therapy. http://www.apta.org/PatientCare/Nutrition. Published 2018. Accessed May 14, 2018.
76. Ferguson M, Capra S, Bauer J, Banks M. Development of a valid and reliable malnutrition screening tool for adult acute hospital patients. Nutrition. 1999;15(6):458–464. doi:10.1016/S0899-9007(99)00084-2.
77. Kyle UG, Kossovsky MP, Karsegard VL, Pichard C. Comparison of tools for nutritional assessment and screening at hospital admission: a population study. Clin Nutr. 2006;25(3):409–417. doi:10.1016/j.clnu.2005.11.001.
78. Rubenstein LZ, Harker JO, Salva A, Guigoz Y, Vellas B. Screening for undernutrition in geriatric practice: developing the Short-Form Mini-Nutritional Assessment (MNA-SF). J Gerontol A Biol Sci Med Sci. 2001;56(6):M366–M372. doi:10.1093/gerona/56.6.M366.
79. White JV, Guenter P, Jensen G, Malone A, Schofield M. 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). J Parenter Enteral Nutr. 2012;36(3):275–283. doi:10.1177/0148607112440285.
80. US Department of Health and Human Services and US Department of Agriculture. 2015-2020 Dietary Guidelines for Americans. 8th ed. Washington, DC: Office of Disease Prevention and Health Promotion, Office of the Assistant Secretary for Health, Office of the Secretary, US Department of Health and Human Services; 2015:18. doi:10.1097/NT.0b013e31826c50af.
81. Academy of Nutrition and Dietetics. MyPlate for Seniors. https://www.eatright.org/for-seniors. Published 2018. Accessed March 6, 2018.
82. Dorner B, Friedrich EK. Position of the Academy of Nutrition and Dietetics: individualized nutrition approaches for older adults: long-term care, post-acute care, and other settings. J Acad Nutr Diet. 2018;118(4):724–735. doi:10.1016/j.jand.2018.01.022.
83. Kamp BJ, Wellman NS, Russell C; American Dietetic Association, American Society for Nutrition, Society for Nutrition Education. Position of the American Dietetic Association, American Society for Nutrition, and Society for Nutrition Education: food and nutrition programs for community-residing older adults. J Am Diet Assoc. 2010;110(3):463–472.
Keywords:

geriatrics; interdisciplinary care; malnutrition; nutrition; physiotherapy; sarcopenia

Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.