Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group

Abstract

The aging process is associated with gradual and progressive loss of muscle mass along with lowered strength and physical endurance. This condition, sarcopenia, has been widely observed with aging in sedentary adults. Regular aerobic and resistance exercise programs have been shown to counteract most aspects of sarcopenia. In addition, good nutrition, especially adequate protein and energy intake, can help limit and treat age-related declines in muscle mass, strength, and functional abilities. Protein nutrition in combination with exercise is considered optimal for maintaining muscle function.
With the goal of providing recommendations for health care professionals to help older adults sustain muscle strength and function into older age, the European Society for Clinical Nutrition and Metabolism (ESPEN) hosted a Workshop on Protein Requirements in the Elderly, held in Dubrovnik on November 24 and 25, 2013. Based on the evidence presented and discussed, the following recommendations are made: (1) for healthy older people, the diet should provide at least 1.0 to 1.2 g protein/kg body weight/day (2) for older people who are malnourished or at risk of malnutrition because they have acute or chronic illness, the diet should provide 1.2 to 1.5 g protein/kg body weight/day, with even higher intake for individuals with severe illness or injury, and (3) daily physical activity or exercise (resistance training, aerobic exercise) should be undertaken by all older people, for as long as possible.

Full text

ESPEN endorsed recommendation
Protein intake and exercise for optimal muscle function with
aging: Recommendations from the ESPEN Expert Group
Nicolaas E.P. Deutz
a
,
*
, Jürgen M. Bauer
b
, Rocco Barazzoni
c
, Gianni Biolo
c
, Yves Boirie
d
,
Anja Bosy-Westphal
e
, Tommy Cederholm
f
,
g
, Alfonso Cruz-Jentoft
h
, Zeljko Krznariç
i
,
K. Sreekumaran Nair
j
, Pierre Singer
k
, Daniel Teta
l
, Kevin Tipton
m
, Philip C. Calder
n
,
o
a
Center for Translational Research in Aging & Longevity, Department of Health and Kinesiology, Texas A&M University, College Station, TX, USA
b
Department of Geriatric Medicine, Carl von Ossietzky University, Klinikum, Oldenburg, Germany
c
Department of Medical, Surgical and Health Sciences, Internal Medicine, University of Trieste, Trieste, Italy
d
Université d’Auvergne, INRA, CRNH, Centre Hospitalier Universitaire, Clermont-Ferrand, France
e
Institut für Ernährungsmedizin, Universität Hohenheim, Stuttgart, Germany
f
Clinical Nutrition and Metabolism, Department of Public Health and Caring Sciences, Uppsala University, Sweden
g
Department of Geriatric Medicine, Uppsala University Hospital, Sweden
h
Servicio de Geriatría, Hospital Universitario Ramón y Cajal, Madrid, Spain
i
Department of Clinical Nutrition, University Hospital Center and School of Medicine, Zagreb, Croatia
j
Division of Endocrinology, Mayo Clinic, Rochester, MN, USA
k
Department of Intensive Care, Institute for Nutrition Research, Rabin Medical Center, Beilinson Hospital, Sackler School of Medicine,
Tel Aviv University, Israel
l
Centre Hospitalier Universitaire Vaudois, Service de Néphrologie, Lausanne, Switzerland
m
Health and Exercise Sciences Research Group, University of Stirling, Stirling, Scotland
n
Human Development and Health Academic Unit, Faculty of Medicine, University of Southampton, Southampton, United Kingdom
o
NIHR Southampton Biomedical Research Centre, University Hospital Southampton NHS Foundation Trust and University of Southampton,
Southampton, United Kingdom
article info
Article history:
Received 9 April 2014
Accepted 9 April 2014
Keywords:
Aging
Nutrition
Protein
Amino acids
Exercise
Sarcopenic obesity
summary
The aging process is associated with gradual and progressive loss of muscle mass along with lowered
strength and physical endurance. This condition, sarcopenia, has been widely observed with aging in
sedentary adults. Regular aerobic and resistance exercise programs have been shown to counteract most
aspects of sarcopenia. In addition, good nutrition, especially adequate protein and energy intake, can help
limit and treat age-related declines in muscle mass, strength, and functional abilities. Protein nutrition in
combination with exercise is considered optimal for maintaining muscle function.
With the goal of providing recommendations for health care professionals to help older adults sustain
muscle strength and function into older age, the European Society for Clinical Nutrition and Metabolism
(ESPEN) hosted a Workshop on Protein Requirements in the Elderly, held in Dubrovnik on November 24
and 25, 2013. Based on the evidence presented and discussed, the following recommendations are made
(a) for healthy older people, the diet should provide at least 1.0e1.2 g protein/kg body weight/day, (b) for
older people who are malnourished or at risk of malnutrition because they have acute or chronic illness,
the diet should provide 1.2e1.5 g protein/kg body weight/day, with even higher intake for individuals
with severe illness or injury, and (c) daily physical activity or exercise (resistance training, aerobic ex-
ercise) should be undertaken by all older people, for as long as possible.
Ó2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
1. New insights in aging and declining muscle function
The natural aging process is associated with gradual and pro-
gressive loss of muscle mass, muscle strength, and endurance, i.e., a
condition called sarcopenia [1]. Such changes have been considered
*Corresponding author. Center for Translational Research in Aging & Longevity,
Department of Health and Kinesiology, Texas A&M University, 1700 Research
Parkway, College Station, TX 77845, USA.
E-mail address: nep.deutz@ctral.org (N.E.P. Deutz).
Contents lists available at ScienceDirect
Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu
http://dx.doi.org/10.1016/j.clnu.2014.04.007
0261-5614/Ó2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Clinical Nutrition xxx (2014) 1e8
Please cite this article in press as: Deutz NEP, et al., Protein intake and exercise for optimal muscle functionwith aging: Recommendations from
the ESPEN Expert Group, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2014.04.007

inevitable consequences of aging. This concept has recently been
challenged, as new study results suggest that mitochondrial
dysfunction, reduced insulin sensitivity, and reduced physical
endurance are related, at least in part, to physical inactivity and to
increases in adiposity rather than to aging alone [2]. The study
results show that regular exercise can help normalize some aspects
of age-related mitochondrial dysfunction, in turn improving muscle
function [2]. Good nutrition, especially adequate protein intake,
also helps limit and treat age-related declines in muscle mass,
strength, and functional abilities. Nutrition in combination with
exercise is considered optimal for maintaining muscle function [3].
With the goal of discussing recent research findings in order to
develop recommendations to help adults sustain muscle strength
and function into older age, the European Society for Clinical
Nutrition and Metabolism (ESPEN) hosted a Workshop with the
ESPEN Expert Group, Protein Requirements in the Elderly, held in
Dubrovnik, Croatia on November 24 and 25, 2013. This article re-
flects practical guidance resulting from the presentations and dis-
cussions during the workshop. The aim of the workshop was to
provide practical guidance for health professionals who care for
older adults, i.e., to recommend optimal protein intake and to
advise age- and condition-appropriate exercise.
We offer practical guidance for maintaining muscle health and
physical function with aging (Table 1). We provide our rationale
and the supporting evidence for these recommendations in the
sections following.
2. Changing protein intake and protein needs in older adults
Compared to younger adults, older adults usually eat less,
including less protein [4,5]. In Europe, up to 10% of community-
dwelling older adults and 35% of those in institutional care fail to
eat enough food to meet the estimated average requirement (EAR)
for daily protein intake (0.7 g/kg body weight/day), a minimum
intake level to maintain muscle integrity in adults of all ages [6].At
the same time, many older adults need more dietary protein than
do younger adults [7,8]. An imbalance between protein supply and
protein need can result in loss of skeletal muscle mass because of a
chronic disruption in the balance between muscle protein synthesis
and degradation [9]. As a result, older adults may lose muscle mass
and strength and eventually experience physical disability [10,11].
In recent years, an ever-increasing body of evidence builds the
case for increasing protein intake recommendations for older
adults (Table 2).
3. Dietary protein intake
There are many reasons older adults fail to consume enough
protein to meet needsdgenetic predisposition to low appetite,
physiological changes and medical conditions that lead to age- and
disease-associated anorexia, physical and mental disabilities that
limit shopping and food preparation, and food insecurity due to
financial and social limitations (Fig. 1)[5].
Table 1
Practical guidance for optimal dietary protein intake and exercise for older adults
above 65 years.
Recommendations
For healthy older adults, we recommend a diet that includes at least 1.0e1.2 g
protein/kg body weight/day.
For certain older adults who have acute or chronic illnesses, 1.2e1.5 g protein/kg
body weight/day may be indicated, with even higher intake for individuals
with severe illness or injury.
We recommend daily physical activity for all older adults, as long as activity is
possible. We also suggest resistance training, when possible, as part of an
overall fitness regimen.
Table 2
Recent studies on protein intake and exercise in older adults.
Study report Study design and key findings
Gray-Donald
et al. 2014 [8]
Prospective, nested case-control study of healthy, community-dwelling adults older than 70 y
Odds ratio of harmful weight loss in participants with low protein intakes (<0.8 g/kg BW/day) was 2.56 compared with participants
with very high protein intakes (1.2 g/kg/day) or 2.15 in participants with moderate protein intakes (0.8e1.0 g/kg BW/day).
Tang et al. 2014 [89] Assessment of protein requirement in octogenarian women using an indicator amino acid oxidation technique (n¼6; tested 3-times
per person)
Based on this method, the mean protein requirement (95% CI) was 0.85 g/kg/day, a requirement 29% higher than the current Estimated
Average Requirement (EAR) for adults. The corresponding adequate protein allowance of 1.15 g/kg/day is 44% higher than the current
Recommended Dietary Allowance (RDA).
Beasley et al. 2013 [11] Longitudinal observational study of a subset of subjects in the Women’s Health Initiative population (n¼5346; women 50e79 years
at baseline; followed 6 years)
Higher protein intake is associated with better physical function and performance and with slower rates of decline in postmenopausal
women.
Breen et al. 2013 [32] Pre-post study experimental design with measures of protein synthesis in healthy older adults (n¼10, age 79 1 yrs) before and
after 14-day reduction of step count
Step reduction leads to reduced muscle mass that is associated with underlying lowering of the response of muscle protein synthesis
to protein ingestion.
Bartali et al. 2012 [90] Longitudinal observational study to examine whether protein intake is associated with change in muscle strength in older adults;
subjects from the InChianti population (n¼598) who were followed for 3 years and had measures of inflammatory markers C-reactive
protein, interleukin-6, and tumor necrosis factor-
a
Lower protein intake was associated with a decline in muscle strength in older adults with high levels of inflammatory markers.
Kim et al. 2012 [60] Randomized controlled trial to evaluate the effectiveness of exercise and amino acid supplementation (high-leucine AAS) in
enhancing muscle mass and strength in community-dwelling elderly sarcopenic women (n¼155, age 75 years)
In sarcopenic women, exercise and AAS together enhance muscle strength, as well as combined variables of muscle mass þwalking
speed and of muscle mass þstrength.
Tieland et al. 2012 [91] A randomized, controlled trial with 2 arms in parallel among frail elderly subjects (n¼62, age 78 1 year); subjects did resistance
exercise twice weekly for 24 weeks and consumed placebo or protein supplements (15 g) twice daily
Prolonged resistance-type exercise training improved strength and physical performance in frail elderly people. Dietary protein
supplementation is required to allow muscle mass gain during such exercise training.
Yang et al. 2012 [36] Dose-response experimental design with measures of protein synthesis in healthy older adults (n¼10, age 79 4yrs) who followed a
bout of resistance exercise with ingestion of 0, 10, 20, and 40 g of whey protein.
In contrast to younger adults, in whom post-exercise rates of muscle protein synthesis are maximized with 20 g of protein, exercised
muscles of older adults respond to higher protein doses of 20 and 40 g protein.
N.E.P. Deutz et al. / Clinical Nutrition xxx (2014) 1e82
Please cite this article in press as: Deutz NEP, et al., Protein intake and exercise for optimal muscle function with aging: Recommendations from
the ESPEN Expert Group, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2014.04.007

4. Dietary protein needs
There are also many reasons older adults have higher protein
needs (Fig. 2). Physiologically, older adults may develop resistance
to the positive effects of dietary protein on synthesis of protein, a
phenomenon that limits muscle maintenance and accretion; this
condition is termed anabolic resistance [12,13]. Mechanisms un-
derlying anabolic resistance and the resultant need for higher
protein intake are: increased splanchnic sequestration of amino
acids, decreased postprandial availability of amino acids, lower
postprandial perfusion of muscle, decreased muscle uptake of di-
etary amino acids, reduced anabolic signaling for protein synthesis,
and reduced digestive capacity [7,12,14]. Older adults likewise have
higher protein needs to offset the elevated metabolism of inflam-
matory conditions such as heart failure, chronic obstructive pul-
monary disease (COPD), or chronic kidney disease (CKD)
undergoing dialysis. In healthy older adults and in a variety of
disease, protein anabolism is related to net protein intake [15].
Most older adults will therefore benefit from higher protein intake.
Further, prolonged disuse of muscle, as with bed rest for illness
or injury, leads to changes in protein synthesis and breakdown,
which cause disuse atrophy of muscle. For example, bed rest for
more than 10 days leads to a decline in basal and postprandial rates
of muscle protein synthesis, especially in older adults [16].
Decreased muscle protein synthesis is the main mechanism for
muscle loss, but there is also indirect evidence that an early and
transient (1e5 days) increase in basal muscle protein breakdown
may contribute to disuse atrophy [16]. While disuse due to acute
illness or injury causes muscle atrophy, so too does physical inac-
tivity due to sedentary lifestyle [17].
In spite of many differences in general health status and phys-
iology of old versus young adults, the recommended dietary
allowance (RDA) has traditionally been set the same for healthy
adults of all agesd0.8 g protein/kg body weight/day [18]. However,
evidence continues to build in favor of increasing this recommen-
dation for optimal protein intake to 1.0e1.2 g/kg body weight/day
for adults older than 65 years [5,7,19,20].
Taken together, evidence shows that when usual dietary protein
intake does not meet increased protein needs of older adults,
negative nitrogen balance results and protein levels decline, espe-
cially skeletal muscle proteins.
5. Consequences of malnutrition and negative nitrogen
balance
In older adults, age- or disease-related malnutrition leads to
negative nitrogen balance and ultimately to frailty and primary or
secondary sarcopenia [1,21]. These conditions can result in
disability, and eventually to loss of independence, falls and frac-
tures, and death [7]. Primary (age-related) and secondary (disease-
related) sarcopenia are difficult to distinguish in older adults
because of the high prevalence of chronic disease in this pop-
ulationd92% after age 65 years, and 95% after age 80 years [22].
Frailty is defined as a biological syndrome with low reserve and low
resistance to biomedical stressors; frailty results from cumulative
declines across multiple biological systems, and worsening frailty is
associated with disability [23]. Physical frailty and sarcopenia are
closely linked [24]. While limited protein intake predicts incident
frailty, it also predicts low bone mass [25,26]. In fact, the presence
of osteoporosis doubles risk for frailty [27]. Notably, frailty can be
prevented or reversed by intervention, particularly by greater
protein intake and exercise [28,29].
6. Physical activity and exercise can maintain or enhance
muscle mass
Loss of muscle mass with aging is primarily due to decreased
muscle protein synthesis rather than to increased muscle protein
breakdown. While the basal level of post-absorptive myofibrillar
protein synthesis may decline with age, this decline is minimal [30].
Inactivity with consequent anabolic resistance are major contrib-
utors to the development of sarcopenia [30]. This concept is sup-
ported by the observation that immobilization induces resistance
of muscle to anabolic stimulation [31]. Similarly, reduction of step
count for two weeks induces anabolic resistance in older adults, as
shown by decreased response of muscle protein synthesis to pro-
tein ingestion, decreased insulin sensitivity, and lowered leg mus-
cle mass [32].
Aging muscle does respond to exercise, especially resistance
exercise. In a classic study of nursing home residents older than 90
years, those who underwent 8 weeks of high-intensity resistance
training experienced significant gains in muscle mass, strength, and
walking speed [33]. A meta-analysis of studies on progressive
resistance training in older adults showed clear benefits for
improved physical function [34]. Resistance exercise may support
these benefits by way of increased insulin sensitivity for [1]
improved glucose utilization [35] and [2] enhanced myofibrillar
protein synthesis [36]. Study results showed that resistanceexercise
was as effective in older adults as it was in young adults to reverse
muscle loss and low muscle protein synthesis [37]. It was recently
suggested that exercise-induced improvement in protein synthesis
may be due to nutrient-stimulated vasodilation and nutrient de-
livery to muscle rather than to improved insulin signaling [38].
In addition, the timing of protein ingestion relative to the ex-
ercise may be important for muscle mass accretion. In a study of
younger adult men, the benefits of resistance exercise on protein
synthesis persisted up to 24 h post-exercise [39]. More research is
needed to delineate mechanisms that link physical activity/nutri-
tion to recovery of lost muscle protein in older adults.
Fig. 1. Protein status: factors leading to lower protein intake in older persons.
Fig. 2. Protein status: factors leading to higher protein needs in older persons.
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Please cite this article in press as: Deutz NEP, et al., Protein intake and exercise for optimal muscle functionwith aging: Recommendations from
the ESPEN Expert Group, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2014.04.007

7. Protein requirements without and with chronic diseases or
conditions
Older adults are expected to benefit from increased dietary
protein intake, especially those with anorexia and low protein
intake along with higher needs due to inflammatory conditions
such as heart failure, COPD, or CKD undergoing dialysis [40].
Further research is needed to identify and develop tools that can
precisely define protein needs in older individuals with chronic
conditions. Research is likewise needed to determine whether
increased protein intake can measurably improve functional out-
comes. The goal for future studies is to identify specific protein and
amino acid needs for older adults, including those who are healthy
and those with diseases common to aging.
8. Optimal protein or amino acid type and amount
A wide range of factors can affect the amount of dietary protein
needed by an older person -digestibility and absorbability of protein
in foods consumed, whether chewing capacity is normal or
impaired, protein quality and amino acid content, sedentary lifestyle
(including immobilization or inactivity due to medical condition),
and presence of stress factors (inflammation and oxidative stress).
8.1. Amount of protein
Debate continues about whether a per-meal threshold amount
of protein intake is needed to stimulate protein synthesis in older
adults [41] or whether protein synthesis is linearly related to pro-
tein intake [15]. Either way, evidence suggests that older adults
who consume more protein are able to maintain muscle mass and
strength [8,10,42,43]. Older adults who consumed 1.1 g protein/kg
body weight/day lost less lean body mass (muscle) than did those
who consumed only 0.7e0.9 g protein/kg body weight/day [10].
Among hospitalized older patients, at least 1.1 g protein/kg body
weight/day was needed to achieve nitrogen balance, and safe
intake was up to 1.6 g protein/kg body weight/day [43].
Recent dietary recommendations for older adults are now
including higher protein intake than for younger adults [7,44]. The
international PROT-AGE study group recommended 1.0e1.5 g pro-
tein/kg body weight/day for individuals older than 65 years [7] with
or without disease, and the new Nordic Nutrition Recommendations
suggest targeting 1.2e1.4 g protein/kg body weight/day with protein
as 15e20% of total energy intake for healthy older adults [44,45].
8.2. Protein source, digestion, and absorption
Properties of the protein itself havethe potentialto affect digestion
and absorption, e.g., whey, a milk protein, is considered a “fast”pro-
tein due to its quick release of aminoacids, while casein, anothermilk
protein, is a “slow”protein [46,47]. In a study by Tang et al., ingestion
of whey protein increased muscle protein synthesis more than casein
[48]. However, it was shown that whey and casein resulted in equally
increased protein synthesis when ingested after resistance exercise
[49]. The difference betweenthese studies is likely due tothe form of
casein used. Micellular casein, a form that leads to slower digestion,
was used by [48], while calcium caseinate was used by [49].
From other perspectives, a person’s poor dentition can limit
chewing capacity and protein availability [50], as can under- or
over-cooking of protein foods [51].
8.3. Protein intake pattern
While terminology used to describe patterns of protein intake
varies, intake patterns in research studies were to “spread”protein
evenly over 4 meals or to deliver protein mostly as a large “pulse”in
a single meal. Results of several studies suggest that the pulse
protein feeding pattern may be useful to improve feeding-induced
stimulation of protein synthesis in older adults [52e54]. These
results are seemingly contradictory tothose suggesting that 4 doses
of 20 g of protein across 12 h is the optimal pattern [55]. It is not
clear whether the discrepancy between these studies is due to age
differences, in inclusion of exercise, or most likely, the fact that
20 g protein is not enough to maximally stimulate muscle protein
synthesis in older adults. Further studies are needed to clarify
optimal patterns of protein intake for older adults, and such studies
must include protein synthesis as well as improvements in muscle
strength and performance as outcome measures.
8.4. Specific amino acids and metabolites
Branched chain amino acids (BCAA), especially leucine, posi-
tively regulate signaling pathways for synthesis of muscle proteins
[56]. A higher proportion of leucine was required for optimal
stimulation of the rate of muscle protein synthesis in older adults,
as compared to younger adults [57]. In adults who were critically ill,
mixed BCAA likewise increased muscle protein synthesis [58,59].In
a randomized, controlled study of exercise and nutrition in older
sarcopenic adult women in the Japanese community, those who
exercised and consumed supplemental amino acids rich in leucine
showed increased leg muscle mass and strength, and faster walking
speed [60]. Moreover, Borsheim et al.demonstrated that older adult
who were given supplemental essential amino acids (EAA) for 16
weeks developed increased muscle mass and improved function,
even in the absence of exercise interventions [61]. However, other
study results showed that long-term leucine supplementation
alone did not increase muscle mass or strength [62,63].
In addition, beta-hydroxy beta-methyl butyrate (
b
-HMB), an
active metabolite of leucine, has been used by athletes to improve
performance [64]. HMB ingestion increased muscle protein syn-
thesis and reduced muscle protein breakdown in young adults in
insulin-independent manner [65]. Further evidence shows that
b
-
HMB may also help increase muscle mass and strength in older
adults and in specific clinical populations (AIDS, cancer), and can
help attenuate muscle loss in patients who are critically ill and
require prolonged ICU care (ICU-acquired weakness) [66e68].
9. Sarcopenic obesity and protein intake
Sarcopenic obesity is a deficiency of skeletal muscle tissue mass
relative to fat tissue (Table 3). Obesity and inactivity contribute to
decreased muscle mass and to lower muscle quality, especially with
aging [69]. Lower muscle quality is attributed in part to infiltration
of fat into the muscle, which affects both muscle strength and
muscle function [70]. Intramyocellular lipid accumulation also re-
duces synthesis of muscle proteins [71].
Working definitions of sarcopenic obesity have been used in
research studies, but there is not yet a universal definition for
clinical practice [72,73]. Sarcopenic obesity is under-diagnosed due
to a lack of agreement on which body composition indices and
cutoff points to use. A suitable definition should be based on a
measure of fat mass along with a measure of skeletal muscle mass
normalized for height (fat-free mass index, FFMI, or appendicular
skeletal muscle mass index, SMI) [74]. Age-specific reference values
are more advantageous because FFMI or SMI may be misleading in
adults of advanced age, in those with severe obesity, or in weight-
reduced obese patients who have more connective tissue relative to
lean mass. A simplified diagnosis of sarcopenic obesity can be based
on a single image of muscle and adipose tissue of the thigh (mag-
netic resonance image or dual X-ray absorptiometry) [74]. This
N.E.P. Deutz et al. / Clinical Nutrition xxx (2014) 1e84
Please cite this article in press as: Deutz NEP, et al., Protein intake and exercise for optimal muscle function with aging: Recommendations from
the ESPEN Expert Group, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2014.04.007

method does have limitations; the ratio of skeletal muscle to fat
tissue varies by sex and by body region in individuals with very
high adiposity [74].
In older adult men and women, low muscle mass and high fat
infiltration into the muscle were associated with decreased
strength and increased risk of losing mobility [70]. Similarly, low
muscle mass correlated with low functionality [70]. The conse-
quences of sarcopenic obesity are serious, including mobility limi-
tations, lower quality of life, and risk of early death [70,75e77].
Therefore, management of sarcopenic obesity aims primarily to
sustain muscle strength and function and secondarily on weight
loss with focus on losing fat but not muscle. Physical exercise is
important in weight loss, as restriction of energy intake is other-
wise likely to induce loss of skeletal muscle [78]. Taken together,
the recommended strategy for management of sarcopenic obesity
is a combination of moderate calorie restriction, increased protein
intake, and exercise (endurance and resistance training).
10. Concerns about negative effects of higher protein intake
in older adults
While the benefits of increased dietary protein are acknowl-
edged for maintenance of muscle health in older adults, health
professionals often express concern that high-protein diets will
stress and worsen declining kidney function in this population.
However, evidence shows that many healthy older adults have
preserved kidney function [79e81]. On the other hand, those older
adults who are unhealthy are more likely to develop mild kidney
insufficiency or CKD. For such individuals with a short life expec-
tancy, nutritional recommendations (such as restriction of dietary
protein intake) should support quality of life in the short-term.
Specifically, when making recommendations for protein intake,
consider the balance between risk of disability/death and risk of
developing end-stage renal disease.
Serum creatinine and creatinine clearance are poor markers of
glomerular filtration rate (GFR) in older adults since these values
are strongly determined by muscle mass, which is reduced in this
population. For recommendation of dietary intake, it is helpful to
use serum creatinine-derived formulas to estimate GFR. The
Modification of Diet in Renal Disease (MDRD) Study equation,
which incorporates information about age, sex, race, and serum
creatinine concentration is most commonly used in clinical practice
and in research studies [82]. However, it systematically under-
estimates GFR in individuals with normal or near-normal GFR
(>60 ml/min/1.73 m
2
). The Chronic Kidney Disease Epidemiology
Collaboration (CKD-EPI) is a new and improved equation to esti-
mate GFR, particularly in individuals with normal GFR (>60 ml/
min/1.73 m
2
)[83]. Although these equations improve the estima-
tion of GFR compared to serum creatinine in older adults, the
MDRD equation still underestimates mean measured GFR by 25%,
and the CKD-EPI equation by 16%, respectively, in this population.
This bias may lead to misclassifying healthy older persons as having
CKD [84]. Based on GFR estimates, kidney function is categorized as
normal or mild dysfunction (GFR >60 ml/min/1.73 m
2
), moderate
dysfunction (30 <GFR <60 ml/min/1.73 m
2
), or severe dysfunction
(GFR <30 ml/min/1.73 m
2
). It is notable that CKD can also result
from defects in kidney structure or kidney function that are evident
as proteinuria or other problems but not as altered GFR [85].
For protein intake in patients with possible alteration of kidney
function, the following guidance is offered:
In older adults with healthy kidneys or with only mild
dysfunction, standard protein intake is safe.
In older patients with moderately impaired GFR or another form of
CKD, physicians customarily assess the balance between risks and
benefits, and use clinical judgment to make recommendations.
In patients with severe CKD, it is usual to recommend a lower
protein intake of 0.6e0.8 g/kg/day with sufficient energy intake
(about 30 kcal/kg/day). However, multi-morbid patients on
palliative care are an exception to this rule. These individuals
may benefit from unrestricted intake of dietary protein because
Table 3
Profile of sarcopenic obesity.
Feature
Definition Deficiency of skeletal muscle relative to fat tissue;
evolving definitions should include measure of
muscle performance too
Prevalence 4%e12% in individuals aged >60 years, depending
on the defining cutoffs used [72]
Health
consequences
Mobility limitations [70]
Reduced quality of life [75]
Risk of mortality [76]
Clinical
management
Weight loss with focus on losing fat but not muscle
Increased dietary protein intake
Resistance training for building muscle and
endurance exercise [75]
• Older adults have greater protein needs to compensate for
anabolic resistance and hypermetabolic disease.
• Older adults may also have decreased intake due to age-related
appete loss, medical condions, financial limits.
•Opmal intake of at least 1.0 to 1.5 g protein/kg BW/day is
recommended; individual needs depend upon the severity of
malnutrion risk.
Dietary
protein intake
• Regular exercise helps maintain skeletal muscle strength and
funcon in older adults.
• Resistance training has limited but posive effects on recovery of
muscle in older people.
• A combinaon of resistance training and adequate dietary
protein/amino acid intake for healthy muscle aging is
recommended.
Exercise
Fig. 3. Recommendations for maintaining healthy muscle with aging.
N.E.P. Deutz et al. / Clinical Nutrition xxx (2014) 1e85
Please cite this article in press as: Deutz NEP, et al., Protein intake and exercise for optimal muscle functionwith aging: Recommendations from
the ESPEN Expert Group, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2014.04.007

the short-term risks associated with protein energy wasting are
greater than the long-term risks of worsening renal function
due to diet with standard protein content.
11. Conclusions
If the increasing life expectancy over the past two centuries
continues at the same rate through the 21st century, many babies
born since 2000 will celebrate their 100th birthdays [86]. In fact,
average lifespan has increased 7e10 years in just 3 decades [86].
What distinguishes a generally healthy, long-lived person
today? A study of Japanese centenarians (100 years or older) found
that those who remained autonomous, i.e., performed activities of
daily living, had good cognition, and had good social networks, had
more frequent intake of protein and regular exercise as dis-
tinguishing features compared to their non-autonomous peers [87].
Adequate dietary protein intake and continuing exercise are
important to healthy aging. Trajectories of greater muscle protein
breakdown are more likely when older age is confounded by acute
or chronic disease, e.g., cancer, heart failure, COPD, or CKD under-
going dialysis. If protein catabolism not offset by increasing protein
intake, along with maintaining physical activity, older adults are at
higher risk for sarcopenia, frailty, disability. Results of a recent
study showed that low dietary protein intake can help prevent
cancer and other diseases in young adults, while older adults need
high protein intake to sustain healthy aging and longevity [88].
In order to help prevent or delay adverse consequences, we
encourage increased intake of dietary protein for older adults (65
years) compared to younger adults, and continued participation in
routine exercise or physical activities (Fig. 3). At the same time, it is
important for older people to balance total energy intake with total
body energy demandsda rationale for consuming protein as a
higher proportion of daily energy intake.
Conflict of interest
None.
Acknowledgments
The authors thank Dr. Cecilia Hofmann (C. Hofmann & Associ-
ates, Western Springs, IL, USA) for her capable assistance with
writing, reference management, and editing.
Work by Nicolaas E. P. Deutz for this article was supported by
Award Number R01HL095903 from the National Heart, Lung, and
Blood Institute. The content is solely the responsibility of this au-
thors and does not necessarily represent the official views of the
National Heart, Lung, and Blood Institute or the National Institutes
of Health.
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