Bales2018-Obesity Interventions For Older Adults - Diet As A Determinant of Physical Function

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Symposium—Health and Disease Implications in

Older Adults Beyond BMI - Composition and


Quality of Body Tissues

Obesity Interventions for Older Adults: Diet as a


Determinant of Physical Function
Connie W Bales1,2,3 and Kathryn N Porter Starr1,2,3
1 Center for the Study of Aging, Duke University Medical Center, Durham, NC; 2 Geriatric Research, Education, and Clinical Center, Durham VA Medical Center,

Durham, NC; and 3 Department of Medicine, Duke University Medical Center, Durham, NC

ABSTRACT
Throughout the world, a high prevalence of obesity in older populations has created a new phenotype of frailty: the obese, functionally frail older
adult. The convergence of the obesity epidemic with global graying will undoubtedly increase the prevalence of this concern. Barriers to treatment
include ambiguities about the appropriate level of obesity that should trigger an intervention, due to age-related physiologic changes and a lack of
consensus on specific criteria and cutoffs. Moreover, obesity interventions for this population have been limited by concerns about negative effects
on lean mass, bone mineral density, and even mortality. However, newly reported approaches for restoring physical function by obesity reduction
have shown good short-term efficacy. Because the majority of these interventions have used exercise as part of the treatment, this review focuses
specifically on current understanding of the discrete effects of dietary interventions for geriatric obesity with regards to functional outcomes on tests
including the Short Physical Performance Battery, the Physical Performance Test, and the Western Ontario and McMaster Universities Osteoarthritis
Index. The literature showed roughly equal benefits to function from a weight reduction diet or exercise regimen, although neither modality was
as efficacious alone as the 2 combined. Only 1 of 3 studies of protein intake during weight loss showed a positive effect of protein on function, but
findings to date are too limited to prove or disprove a protein benefit. We conclude that although diet and exercise should be combined whenever
possible, it remains important to further investigate the beneficial and likely unique effects that calorie restriction and/or nutrient modification can
provide, particularly for obese and functionally frail older populations. Adv Nutr 2018;9:151–159.

Keywords: calorie restriction, obesity reduction, older adults, function

Introduction on health, independence, and quality of life in older adults is


A global epidemic of obesity has combined with an unprece- multifaceted, but the primary focus of this review is on the
dented “graying” of the population to threaten the health and impact of diet interventions on physical function outcomes
functional independence of future cohorts of older adults. in obese older individuals. The deterioration of functional
Already, almost 40% of US adults aged ≥60 y have a BMI status severely impacts quality of life for obese older adults,
(in kg/m2 ) exceeding 30 (1). Increases in obesity are also be- increasing their risk of falls and other injuries and enhanc-
ing recorded globally, with rates of 10–15% in the developing ing the likelihood of institutionalization (4–6). Unless effec-
world (2). The combination of obesity with age-related eleva- tive obesity interventions can be found, the functionally dis-
tions in metabolic and functional risk contributes to physical abled, obese older adult may become the “most commonly
limitations and reduced independence, as well as a host of encountered phenotype of frailty” in the near future (7). This
chronic cardiometabolic disorders (3). The impact of obesity concern has begun to be addressed in a number of obesity
intervention trials aimed at lessening associated comorbidi-
This article is a review from the symposium “Health and Disease Implications in Older Adults
Beyond BMI - Composition and Quality of Body Tissues” held April 24, 2017 at the ASN
ties, preserving lean mass, and/or improving function, many
Scientific Sessions and Annual Meeting at Experimental Biology 2017 in Chicago, IL. of which have been recently reviewed (8–13). The majority of
Address correspondence to KNPS (e-mail: [email protected]). these interventions have emphasized exercise as an essential
Supported by the United States (U.S.) Department of Veterans Affairs Rehabilitation Research
and Development Service Program (CDA-2/ IK2 RX002348), and National Institute of Health
modality of treatment and focused on lean mass preservation
(P30 AG028716). as an outcome; very few have been designed to examine the
Author disclosures: CWB and KNPS, no conflicts of interest. discrete effects of diet interventions on physical function as
Abbreviations used: FSQ, Functional Status Questionnaire; IDEA trial, Intensive Diet and Exercise
for Arthritis; MEASUR-UP, Measuring Eating, Activity, and Strength: Understanding the
an outcome. While the benefits of exercise for cardiovascu-
Response—Using Protein; PPT, Physical Performance Test; SPPB, Short Physical Performance lar health and muscle strength are robust and well substanti-
Battery; WOMAC index, Western Ontario and McMaster Universities Osteoarthritis Index. ated (14, 15), the role of diet in obesity treatment is equally

Published by Oxford University Press on behalf of the American Society for Nutrition 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. Adv Nutr
2018;9:151–159; doi: https://doi.org/10.1093/advances/nmx016. 151
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crucial but under-studied. Following a discussion of the up- medical treatments riskier and hastens the need for in-
surge of obesity prevalence in older adults and its implica- stitutionalization due to loss of functional independence.
tions for health and physical function, the intent of this nar- Functionally frail, obese older adults have a much greater
rative review is to summarize current understanding of the likelihood of getting admitted to a nursing home than do
effects of diet apart from exercise with regards to physical nonobese elders (23). Yet, studies of potential interventions
function outcomes in obese older adults. are hampered due to the lack of consensus on the specific
criteria most indicative of sarcopenic obesity. Thus, esti-
The Convergence of Global Graying with the mated rates of prevalence of sarcopenic obesity range widely
Obesity Pandemic depending upon the definition employed (24), with findings
Thanks to lower birth rates and tremendous strides in treat- of ≤84% in men and 94% in women in an analysis of DXA
ment and prevention of infectious diseases, “global graying” results from the NHANES (National Health and Nutrition
is now occurring in rapid fashion. In the United States, the Examination Survey) of 1999–2004.
population of adults aged ≥65 y will nearly double to almost
83 million by 2050, up from ∼43 million in 2012 (16). Glob- Impact of obesity in later life on physical function
ally, demographic milestones are rapidly being realized. For The negative impact of sarcopenic obesity on health and
the first time in recorded history, adults aged >65 y will soon functional independence underscores the importance of
outnumber those aged ≤5 y; this “crossing over” is unprece- identifying interventions that reverse physical deficits; it also
dented in recorded human history and it will continue into explains why this review focuses on studies of physical func-
2050, when there will be twice as many older adults as chil- tion outcomes rather than on intervention effects on lean
dren aged ≤5 y (17). mass per se. Some terms commonly used to describe the
Another dramatic global trend is obesity in later life, quality and performance of muscle, along with descriptions
which was rare until recently but has become an important of functional tests discussed in this paper, are shown in
harbinger of nutritional risk in many older persons (1). This Table 1. In Figure 1, we see that both aging and obesity are
trend is driven by an overall pandemic of obesity (2). World- consistently associated with poor muscle quality (25) and re-
wide obesity has more than doubled since 1980, with >600 sulting deterioration of muscle function (26). With aging,
million adults (13%) being obese. In much of the world, be- sarcopenia, a progressive loss of muscle mass and strength,
ing overweight or obese now contributes more to mortality almost inevitably occurs (27, 28). Lean muscle mass declines
than being underweight (18). from ∼50% of total body weight in young adults to ∼25% at
75–80 y of age (29). This progressive deterioration of muscle
Indicators of obesity in older adults quantity and quality leads to slower movement, a decline in
In order to understand the impact of obesity in later life, it strength and power, and increased risk for falls (30). Through
is important to note the limitations of current approaches to different mechanisms, obesity is also strongly associated with
assessment of excess adiposity in this population. Typically, deterioration of muscle quality and loss of physical func-
BMI measurement is used to classify obesity, despite the well- tion. Adiposity favors the accumulation of lipids between and
known limitations of this index for use in older persons. BMI within muscles (reduced muscle quality), as well as a persis-
does not fully capture the extent of adiposity because as adults tent low-grade inflammation (due to chronic activation of the
age, they accumulate a greater proportion of body weight as innate immune system) that also leads to muscle depletion
fat compared with lean tissue (19). Additionally, BMI does by enhancing protein breakdown and impairing myogenesis
not capture the tendency of older adults to accumulate more (11, 31). In addition, with the reduced ability to be physi-
intra-abdominal than subcutaneous or whole body fat and cally active as a result of both obesity and aging, progressive
the commonly observed loss of height with aging due to ver- muscle atrophy due to disuse takes place (32). Thus, the con-
tebral body compression and spinal kyphosis can also distort vergence of obesity with aging dramatically accelerates func-
the BMI measurement. The use of waist circumference as an tional decline and results in a marked threat to independence
indicator of visceral adiposity has been suggested (>102 cm for present and future cohorts of older adults.
in men and >88 cm in women), although there are no age-
specific recommendations (20). It should also be noted that The Controversial Nature of Obesity
ethnic differences in BMI cutoffs associated with detrimental Interventions for Older Adults
health changes have been noted, although these differences Given the many adverse effects of obesity on health and well-
have not been well described in older adults (21, 22). being in older adults, it would seem logical to advocate for
Another way to classify detrimental changes in body more interventions targeting weight reduction for this pop-
composition in older adults is by the diagnosis of sarcopenic ulation. In fact, specific recommendations for obesity treat-
obesity. Broadly speaking, sarcopenic obesity refers to the ment in older adults have advised a cautious approach (33).
common phenomenon wherein sarcopenia (decreased Weight reduction can be difficult to achieve in older adults,
muscle mass and function) co-occurs with obesity (excess who have lower basal metabolic rates, calorie requirements,
body fat mass) (20). Sarcopenic obesity is linked with a host and physical activity (34–36) and may have greater reduc-
of metabolic health problems as well as disabilities, falls, tions in energy expenditure during weight loss (37). More-
and mobility limitations (20). It makes surgery and other over, efforts to reduce body weight in obese older adults raise

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TABLE 1 Glossary of muscle physiology descriptors and functional tests applied in older adults
Terminology
Muscle physiology
Muscle strength The ability of a muscle or muscle group to develop maximal contractile force against a resistance in a single
contraction. Muscle strength may be measured using a one-repetition maximum, which is the sum of the
maximal weights lifted in the biceps curl, bench press, seated row, knee extension, knee flexion, and leg press
exercises.
Muscular endurance The ability of a muscle or muscle group to exert submaximal force for extended periods of time. Exercises such as
running illustrate muscular endurance as they require multiple repetitions of an exercise.
Muscle quality Typically defined as muscle strength or power per unit of muscle mass, muscle quality is a complex characteristic
determined by a variety of attributes, including muscle size and architecture, fiber type, contractile properties,
aerobic capacity, and intermuscular adipose tissue (25).
Sarcopenia The loss of muscle mass and muscle strength that is associated with aging; features include decreased muscle
mass and muscle cross-sectional area and infiltration of muscle with fat and connective tissue (28).
Muscle wasting A degree of muscle atrophy associated with clinically important impairments in functional capacity and/or
increased risk of morbidity or mortality. Also referred to as myopenia (32), it is a distinct condition from sarcopenia.
Functional tests
Short Physical Performance Battery The SPPB (74) is a performance-based test designed to assess mobility in older adults by measuring 3 categories
scored on a scale of 0 to 4—balance, strength, and gait speed. There are 3 different standing balance tests
(side-by-side, semi-tandem, and tandem), 5 chair stands, and a 4-meter walk. Performance in each category is
scored on a scale of 0 to 4 with a total score ranging from 0 to 12.
Physical Performance Test The PPT assesses performance of tasks that simulate activities of daily living. It includes 7 standardized tasks
(walking 50 ft, putting on and removing a coat, picking up a penny, standing up from a chair, lifting a book,
climbing 1 flight of stairs, and performing a progressive Romberg test) plus 2 additional tasks (climbing up/down
4 flights of stairs and performing a 360-degree turn). The score for each task ranges from 0 to 4; a perfect score is
36 (52).
Western Ontario and McMaster The WOMAC Index is a widely used set of standardized questionnaires originally designed to assess symptoms
Universities Osteoarthritis Index and physical disability in individuals with osteoarthritis of the hip and/or knee (53). It includes assessment of pain,
stiffness, and physical function.

strong concerns about the concomitant loss of lean body uptake and tolerance (39). The inclusion of an exercise pro-
mass. Of total weight lost, ≥25% is likely to be lost as lean gram with weight reduction treatment can help minimize
mass (38). Any loss of lean mass in older individuals is a the loss of lean mass, although the long-term impact of
concern for future functional status, as well as for glucose various weight-loss strategies in this population is not well

FIGURE 1 Both aging and obesity are associated with poor muscle quality and a reduction of muscle function. Decreased muscle
endurance, elevated pro-inflammatory cytokines, and infiltration of fat into muscle combine with muscle disuse to reduce overall muscle
quality and worsen physical function.

Obesity interventions for older adults 153


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characterized. Furthermore, not all obese older adults are Function. To date, only a few trials of obesity reduction in
able or willing to sustain a regular program of exercise. older adults that included a diet-alone arm have reported
As subsequently discussed, another concerning observation function as an outcome. As shown in the first 3 studies on
during obesity reduction in older adults is a slight loss of bone Table 2, these trials range from 12 to 18 mo in duration (14,
mineral density; this occurs as a consequence of weight loss 47–51). Villareal et al. (14) explored the independent and
in adults of all ages and its long-term impact on fracture risk combined effects of a weight management diet and an ex-
is unknown (40). ercise treatment in older adults aged ≥65 y. Physical Per-
The well-characterized “obesity paradox” is yet another formance Test (PPT) (52) scores were best in the combi-
concern related to the controversy about obesity reduction nation group, while improvements in the diet-only group
in later life. Several chronic health conditions associated with for PPT were similar to those of the exercise-only treatment
aging have the potential to progress to conditions of wasting, group. Functional Status Questionnaire (FSQ) improvements
also known as cachexia (41). The “reverse epidemiology” of were greater in the combination group compared with the
obesity or “obesity paradox” has been observed in such indi- diet-only group. In the Arthritis, Diet, and Activity Promo-
viduals, meaning that often those with a higher BMI survive tion Trial (ADAPT) including overweight and obese older
longer than those with a lower BMI. This phenomenon has adults with osteoarthritis, Messier et al. (48) compared long-
been confirmed in the case of cancer cachexia (42), end stage term (18 mo) exercise and diet-induced weight loss sepa-
renal disease (43), and chronic heart failure (44), as well as a rately or in combination with a healthy lifestyle control group
number of other common chronic conditions. The availabil- with regards to physical function and mobility. The diet plus
ity of larger body stores of both energy (fat) and lean mass, exercise group improved in both the 6-min walk distance and
as well as a better nutritional state overall is thought to con- stair climb, while the exercise-only group improved in the
tribute to increased survival in obese older individuals (45). 6-min walk distance compared with the healthy lifestyle con-
While this potential benefit of obesity on mortality is well rec- trol group. The diet-only group did not improve in either
ognized, the fact remains that severe decrements in function mobility measure compared with the health lifestyle control
because of obesity could translate into years of disability dur- group. In another trial by these investigators, the Intensive
ing an extended lifetime (20). For all these reasons, and as Diet and Exercise for Arthritis (IDEA) trial, Messier et al.
emphasized in a 2016 review by Locher et al. (8), the overall (47) again studied overweight and obese older adults with
safety of weight-loss interventions for those aged ≥65 y re- osteoarthritis over an 18-mo duration. The IDEA trial as-
mains controversial and yet in great need of study because of sessed function and mobility as secondary outcomes of an
the pervasiveness of the obesity problem. intensive diet-induced weight loss with or without exercise.
These investigators found a better Western Ontario and Mc-
Master Universities Osteoarthritis Index (WOMAC) score
Findings on Obesity Reduction and Function
(53) in the combination group than in the diet-only and
Outcomes: Diet-based Interventions
exercise-only groups; the diet-only and exercise-only groups
The effectiveness of exercise as part of obesity interventions
improved but did not differ from each other. The 6-min walk
in older adults has been investigated and confirmed in a num-
distance results were better for both the combination and
ber of trials. Almost all recent studies of weight reduction in
the exercise group than for the diet group. The combination
this population have included exercise in all treatment arms,
group had faster walking speeds compared with the exercise-
with the best results being reported in study arms that com-
only group; there was no difference between the diet-only and
bine both exercise and a calorie-restricted diet (12, 46). The
exercise-only groups for walking speed.
results of these studies have been recently summarized (8, 10,
11, 38).
Higher-protein weight-loss diets
There is a strong consensus that the protein requirement
Calorie-restricted weight-loss diets of older adults exceeds the RDA of 0.8 g protein · kg body
Weight-loss outcomes. In head-to-head studies of diet weight−1 · d−1 , with the suggestion for intakes ranging
compared with exercise, calorie-restricted diet regi- ≤1.5 g protein · kg body weight−1 · d−1 or more in high-
mens almost always result in more weight loss than do risk situations (54, 55). Protein intakes exceeding the RDA
exercise-alone treatments (14). As shown in Table 2, amounts have been linked with better preservation of lean
exercise treatments without a diet component typically mass (56, 57) and recent findings from the Framingham
result in little or no weight loss, while calorie-restricted study have confirmed the benefits of high-quality (animal)
diets achieve mean reductions in baseline body weight protein for protection of appendicular lean mass (58), preser-
of 5% to almost 10%. Other benefits may accrue: in the vation of grip strength (59), and decreased risk of function
recently reported CROSSROADS (Calorie Restriction decline in the long term (60). Muscle becomes more resistant
in Overweight SeniorS: Response of Older Adults to a to anabolic stimulation with age, but there is encouraging
Dieting Study) trial, Ard et al. (46) found that an exercise evidence that generous and balanced intakes of high-quality
regimen plus weight-loss diet was more successful at reduc- (complete) protein can offset age-related anabolic resis-
ing body fat and improving cardiometabolic risk factors than tance in the aging muscle (61–63). As confirmed in several
exercise alone. short-term studies, essential amino acids, especially leucine,

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TABLE 2 Randomized controlled trials of obesity reduction with a diet treatment arm: weight loss and function-related outcomes1
Study reference Population Interventions tested Findings
Calorie restriction
Messier et al. (2013) n = 454 Arms: Weight: Diet loss (9.5%) and Diet + Ex (11.4%) were significantly
(IDEA trial) (47) BMI = 33.6 ± 3.7 Ex greater than Ex loss (2.0%) (P < 0.001).
Age = 66.0 ± 6.0 y Diet Function: WOMAC function score significantly increased in Diet + Ex
Sex = 72% F Diet + Ex compared with Diet (P = 0.003) and Ex (P < 0.001). For the 6MWT,
Description: Knee OA Duration: 18 mo Diet + Ex arm walked significantly farther than both Diet arm
(P < 0.001) and Ex arm (P = 0.005). The Ex arm walked significantly
farther than the Diet arm (P = 0.009). Walking speeds significantly
increased in Diet + Ex compared with Ex (P = 0.003), no difference
was found between Diet + Ex and Diet arms.

Villareal et al. (2011) n = 107 Arms: Weight: Diet loss (10%) and Diet + Ex loss (9%) were significantly
(14) BMI = 37.2 ± 5.0 Control greater than Ex loss (1%) and Control loss (<1%) (P < 0.001).
Age = 69.7 ± 4.0 y Diet Function: PPT score significantly increased in all 3 intervention arms at
Sex = 63% F Ex 12 mo (P < 0.001). PPT score increased significantly more in the
Description: Mild to Diet + Ex Diet + Ex arm compared with Diet arm (P < 0.001) and Ex arm
moderate frailty Duration: 12 mo (P = 0.04). Following 12 mo, FSQ significantly increased in all 3
intervention arms (P < 0.01). Diet + Ex FSQ score increased
significantly more than Diet FSQ score (P = 0.04).
Messier et al. (2004) n = 316 Arms: Weight: Diet loss (4.9%) and Diet + Ex loss (5.7%) were significantly
(ADAPT trial) (48) BMI = 34.2 ± 0.6 Control greater than Control (1.2%) (P < 0.05).
Age = 68.7 ± 0.8 y Diet Function: Diet + Ex arm significantly improved more in both 6MWT
Sex = 68% F Ex and stair climb time compared with Control (P < 0.05). Ex group
Description: Knee OA Diet + Ex significantly improved in 6MWT compared with Control (P < 0.05).
Duration: 18 mo No difference between Diet and Control arms for either mobility
measure.
Calorie restriction plus nutrient modification
Porter Starr et al. n = 67 Arms: Weight: Total body weight significantly decreased for both arms
(2016) BMI = 36.9 ± 6.3 Control (NP Diet) (P < 0.001). Control (7.5%) and HP Diet (8.1%) losses were not
(MEASUR-UP trial) Age = 68.3 ± 5.6 y HP Diet different (P = 0.52).
(49) Sex = 79% F Duration: 6 mo Function: SPPB scores significantly increased in HP Diet more than in
Description: SPPB score Control (P < 0.05). Hand grip strength was unchanged for both
4–10 arms (P = 0.53).
Bales et al. (2017) n = 80 Arms: Weight: Total body weight significantly decreased for both arms
(POWR-UP trial) (50) BMI = 37.8 ± 5.9 Control (NP Diet) (P < 0.001). Control (6.3%) and HP Diet (6.2%) losses were not
Age = 60 ± 8.2 y HP Diet different (P = 0.92).
Description: Women Duration: 6 mo Function: 6MWT distance increased in Control (P < 0.01) and HP Diet
only (P < 0.001) with no difference between groups. SPPB and
8-ft-up-and-go significantly improved in both arms (P < 0.01) with
no group difference. 30-s chair stand significantly improved in HP
Diet (P < 0.01), but no between-group difference was found.
Backx et al. (2016) n = 61 Arms: Weight: Total body weight significantly decreased for both arms
(51) BMI = 31.2 ± 3.0 Control (NP Diet) (P < 0.01). Control (–8.9 kg) and HP Diet (–9.1 kg) losses were not
Age = 63.0 ± 4.8 y HP Diet different (P = 0.58).
Sex = 41% F Duration: 3 mo Function: 1-RM leg press significantly decreased in both arms
Description: lean body (P < 0.01). No change in SPPB score for either arm. 1-RM leg
mass extension significantly decreased in Control (P < 0.01), but no
between-group difference was found. Hand grip strength
significantly decreased in HP Diet (P < 0.01), but no between-group
difference was found. 400-m walking velocity increased in HP
Diet (P < 0.01), but no between-group difference was found.
1
ADAPT, Arthritis, Diet, and Activity Promotion Trial; Diet, Calorie-restricted diet with no exercise treatment; Ex, exercise of any type; FSQ, Functional Status Questionnaire; HP,
high-protein diet; IDEA, Intensive Diet and Exercise for Arthritis; MEASUR-UP, Measuring Eating, Activity, and Strength: Understanding the Response—Using Protein; NP, normal
protein diet; OA, osteoarthritis; POWR-UP, Protein Optimization in Women Enables Results—Using Protein; PPT, Physical Performance Test; SPPB, Short Physical Performance
Battery; WOMAC, The Western Ontario and McMaster Universities Osteoarthritis Index; 6MWT, 6-min walk test.

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initiate the mTOR signaling pathway and stimulate muscle group difference from the normal protein treatment was de-
protein synthesis (64–66). These short-term studies support tected. Other functional improvements included increases in
a balanced, generous intake of protein throughout the day for SPPB and 8-ft-up-and-go results in both the normal and high
optimal protein synthesis in the aging muscle (67, 68). There protein groups, with no group difference.
is a refractory period during which muscle protein synthesis
stimulated by amino acid influx cannot be stimulated again, Weight-loss diets with other nutrient modifications
the so-called “muscle full” phenomenon (26, 69), so that Studies of weight loss with manipulation of nutrients other
balanced protein intake, rather than skewing most of the than protein are rare, and none were identified that studied
protein intake to an evening meal, has been associated with diet apart from exercise effects. Second to protein, vitamin
better outcomes. D is the nutrient of most interest with regards to function.
It has been hypothesized that higher protein intake during Inadequate vitamin D intake has been associated with
obesity reduction may reduce the risk of physical frailty by reduced muscle mass and strength, reduced balance, gait
increasing muscle anabolism; improvements in muscle qual- impairments, and increased risk of falling (20, 75, 76). Thus,
ity may also result (25, 56, 68, 70, 71). Recommendations for vitamin D has begun to be explored as an adjunct to obesity
obesity reduction in older adults have long included advice treatment, although none of the studies we reviewed had
for a protein intake of 1.0 g protein · kg body weight−1 · d−1 a diet-alone arm. Verreijen et al. (77) found a beneficial
(36), albeit without a strong body of high-quality support- effect of a whey protein-, leucine-, and vitamin D–enriched
ing evidence. A recent systematic review and meta-analysis regimen for appendicular lean mass compared with an
addressed the impact of dietary protein intake on body com- iso-caloric control (both groups also performed resistance
position in overweight and obese older adults (13). The re- exercise). Function-related outcomes were not reported. Ma-
sults indicated a small but significant preservation of lean son et al. (78) studied vitamin D supplementation (2000 IU/d
mass with high protein intake during weight loss. The re- compared with placebo) in obese postmenopausal women
view did not address function as an outcome. Additionally, with insufficient concentrations of serum 25-hydroxyvitamin
of the 19 papers included, only 2 trials studied populations D during a 12-mo weight-loss trial that included moderate-
with a mean age of ≥60 y; of these, one study (72) did not to vigorous-intensity aerobic exercise in both groups. The
measure function as an outcome and the other (73) did not vitamin D supplementation did not provide any added pro-
include a diet-alone arm. We are aware of only 3 weight- tection for lean mass or bone mineral density and was associ-
loss studies that have investigated protein intakes exceeding ated with decreased leg strength measured by one-repetition
the current RDA of 0.8 g protein · kg body weight−1 · d−1 strength testing. One suggested explanation for this unex-
with assessment of functional outcomes. The second sec- pected outcome was the possibility that some participants
tion of Table 2 describes these studies. Porter Starr et al. exerted inconsistent amounts of effort on the leg-strength
(74) studied obese men and women who were aged ≥60 y test at the end of the study compared with baseline (78).
and with a suboptimal Short Physical Performance Battery
(SPPB) score, testing a 6-mo diet intervention that compared Summary of findings on diet to date
generous servings of high-quality protein products at each The findings from the trials shown in Table 2 permit only
meal with a normal-protein weight-loss diet (49). Weight preliminary conclusions. Although the trials are of high
loss was achieved equally well in each group and the SPPB quality, the limited number of studies and differences in
score (primary outcome) improved in both groups, with a the target populations and primary outcomes measured for
significantly greater increase (P = 0.02) in SPPB score in function reduce the ability to draw conclusions about diet
the high protein (+2.4 ± 1.7 units) compared with the nor- effects. Generally, the findings for effects of calorie-restricted
mal protein (+0.9 ± 1.7 units) arm. Backx et al. (51) also diets on function were positive and not significantly different
studied protein intake (1.7 compared with 0.9 g protein · kg from the functional benefits yielded by exercise alone. Study
body weight−1 · d−1 ) during a calorie-restricted diet in older findings for high compared with normal protein intake
women and men. The trial was of shorter duration (12 wk) were also too limited to prove or disprove a benefit. Only
and included overweight as well as obese participants. Weight 1 of the 3 studies, Porter Starr et al. (49), showed a clear
loss was successful in both study arms and both arms showed protein benefit. However, the 2 trials showing no group
improvement in 400-m walking speed with no group differ- effect had a lower baseline age (60 ± 8.2 and 63.0 ± 4.8 y
ence. However, leg strength decreased in both groups with no compared with 68.3 ± 5.6 y in Porter Starr et al.) and the
group difference. Using the same protocol as the Porter Starr Bales et al. trial studied only women; thus, it is possible that
et al. trial of enhanced meal intake of high-quality protein age and/or sex might influence the potential that higher
(49), Bales et al. (50) compared normal- and high-protein in- protein intake would be advantageous. Based on the strong
take weight-loss regimens in obese women aged ≥45 y (mean evidence in other literature supporting a protein benefit to
age = 60 ± 8.2 y) during a 6-mo intervention. Weight loss was function in older adults, further studies in obese individuals
achieved in both groups with no group difference. The dis- aged ≥65 y, sufficiently powered to detect differences by
tance walked in 6 min (primary outcome) increased in both sex, are warranted. Regarding other nutrients that might
the normal (P < 0.01) and high (P < 0.001) protein diets, be linked with better function, very little is known. Initial
with no group difference. While 30-s chair stand score sig- findings with vitamin D have yielded mixed results but
nificantly improved in the high protein group (P < 0.01), no are too limited to answer questions about benefit. Even
156 Bales and Porter Starr
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less is known about other nutrients but a recent systematic References
review has examined the possible role of essential minerals 1. Flegal KM, Kruszon-Moran D, Carroll MD, Fryar CD, Ogden CL.
in prevention and treatment of sarcopenia, including out- Trends in obesity among adults in the United States, 2005 to 2014. JAMA
2016;315(21):2284–91.
comes for muscle strength and physical performance (79). 2. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C,
Mullany EC, Biryukov S, Abbafati C, Abera SF,, et al. Global, regional,
and national prevalence of overweight and obesity in children and
Comments on Bone Health and Obesity adults during 1980–2013: a systematic analysis for the Global Burden
While beyond the scope of this review and under-studied for of Disease Study 2013. Lancet 2014;384(9945):766–81.
long-term impact, the potential threat of weight reduction 3. Amarya S, Singh K, Sabharwal M. Health consequences of obesity in the
to bone mineral density needs to be assessed and accounted elderly. J Clin Gerontol Geriatr 2014;5(3):63–7.
4. Jensen GL. Obesity and functional decline: epidemiology and geriatric
for. Fractures and fear of falling greatly increase the risk of
consequences. Clin Geriatr Med 2005;21(4):677–87.
functional frailty in seniors. The conventional wisdom that 5. Rolland Y, Lauwers-Cances V, Cristini C, Abellan van Kan G, Janssen I,
obesity is protective of bone has recently been challenged by Morley JE, Vellas B. Difficulties with physical function associated with
evidence that it is associated with lessened bone quality, rais- obesity, sarcopenia, and sarcopenic-obesity in community-dwelling
ing the possibility that small losses of bone during obesity re- elderly women: the EPIDOS (EPIDemiologie de l’OSteoporose) study.
Am J Clin Nutr 2009;89(6):1895–900.
duction could lead to subsequent fractures (80). Von Thun
6. Vincent HK, Vincent KR, Lamb KM. Obesity and mobility disability in
et al. (81) assessed 42 postmenopausal women 2 y after they the older adult. Obes Rev 2010;11(8):568–79.
started a 6-mo weight-loss trial and reported that they had 7. Alley DE, Ferrucci L, Barbagallo M, Studenski SA, Harris TB. A research
not recovered bone mineral density at that follow-up, irre- agenda: the changing relationship between body weight and health in
spective of whether or not weight regain had occurred. While aging. J Gerontol A Biol Sci Med Sci 2008;63(11):1257–9.
8. Locher JL, Goldsby TU, Goss AM, Kilgore ML, Gower B, Ard JD.
exercise helps to preserve bone, bone-supporting nutrients
Calorie restriction in overweight older adults: do benefits exceed
may also be critically important. In a study of very low calorie potential risks? Exp Gerontol 2016;86:4–13.
diets in obese adults aged ≥65 y, Haywood et al. (82) reported 9. Gill LE, Bartels SJ, Batsis JA. Weight management in older adults. Curr
small but significant losses of total bone density, despite a su- Obes Rep 2015;4(3):379–88.
pervised exercise program thrice weekly. However, the value 10. Batsis JA, Gill LE, Masutani RK, Adachi-Mejia AM, Blunt HB, Bagley
PJ, Lopez-Jimenez F, Bartels SJ. Weight loss interventions in older adults
of good nutrition for bone quality during calorie restriction
with obesity: a systematic review of randomized controlled trials since
over time has also been reported (83). 2005. J Am Geriatr Soc 2017;65(2):257–68.
11. Porter Starr KN, McDonald SR, Bales CW. Obesity and physical frailty
in older adults: a scoping review of lifestyle intervention trials. J Am
Summary Med Dir Assoc 2014;15(4):240–50.
This literature review provided indications that weight-loss 12. Porter Starr KN, Bales CW. Excessive body weight in older adults. Clin
diets may benefit function in this high-risk population of Geriatr Med 2015;31(3):311–26.
13. Kim JE, O’Connor LE, Sands LP, Slebodnik MB, Campbell WW. Effects
obese older adults. It is clear that a reduced calorie intake is
of dietary protein intake on body composition changes after weight
necessary to achieve physiologically important losses of body loss in older adults: a systematic review and meta-analysis. Nutr Rev
weight and, while concerns about loss of lean mass remain, 2016;74(3):210–24.
functional benefits do result when weight loss is achieved. 14. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-
Certainly, a striking shortage of published research prevents Villareal R, Napoli N, Qualls C, Shah K. Weight loss, exercise, or
both and physical function in obese older adults. N Engl J Med
clinical application at this juncture. Evidence of a protein
2011;364(13):1218–29.
benefit apart from exercise is even more limited, although 15. Villareal DT, Aguirre L, Gurney AB, Waters DL, Sinacore DR, Colombo
there is strong support in the literature for further study. De- E, Armamento-Villareal R, Qualls C. Aerobic or resistance exercise, or
spite our limited understanding to date, it is likely that diet both, in dieting obese older adults. N Engl J Med 2017;376(20):1943–55.
interventions provide valuable benefits to physical function 16. He W, Goodkind D, Kowal P. International Population Reports,
P95/16-1, An aging world: 2015. U.S. Census Bureau, editors.
and independence in obese older adults. And, while combin-
Washington, DC: U.S. Government Publishing Office; 2016.
ing diet with exercise whenever possible is optimal, it remains 17. United Nations, Department of Economic and Social Affairs,
important to understand the beneficial and likely unique ef- Population Division [Internet]. World population prospects: the
fects that calorie restriction and/or nutrient modification can 2010 revision, volume I: comprehensive tables. ST/ESA/SER.A/313;
provide. The influence of diet composition in this context is 2011 [cited 2017 Aug 14]. Available from: http://www.un.org/
en/development/desa/population/publications/pdf/trends/WPP2010/
woefully under-studied and future trials with study designs
WPP2010_Volume-I_Comprehensive-Tables.pdf.
that allow the separate examination of exercise and diet ef- 18. World Health Organization [Internet]. Obesity and overweight
fects, especially targeting nutrients likely to be key for phys- factsheet; 2016 [cited 2017 Aug 14]. Available from: http://www.
ical function, are of critical importance. Moreover, both diet who.int/mediacentre/factsheets/fs311/en/.
and exercise interventions need to be studied over the long 19. Newman AB, Lee JS, Visser M, Goodpaster BH, Kritchevsky SB,
Tylavsky FA, Nevitt M, Harris TB. Weight change and the conservation
term (e.g., ≥2 y) to evaluate their lasting impact on functional
of lean mass in old age: the Health, Aging and Body Composition Study.
independence and health-related quality of life. Am J Clin Nutr 2005;82(4):872–8; quiz 915–6.
20. Goisser S, Kemmler W, Porzel S, Volkert D, Sieber CC, Bollheimer
LC, Freiberger E. Sarcopenic obesity and complex interventions
Acknowledgments with nutrition and exercise in community-dwelling older persons—a
All authors have read and approved the final manuscript. narrative review. Clin Interv Aging 2015;10:1267–82.

Obesity interventions for older adults 157


Downloaded from https://academic.oup.com/advances/article-abstract/9/2/151/4969261
by guest
on 29 April 2018
21. Chan RSM, Woo J. Prevention of overweight and obesity: how effective and meta-analysis of randomized controlled trials. Osteoporos Int
is the current public health approach. Int J Environ Res Public Health 2016;27(9):2655–71.
2010;7(3):765–83. 41. Evans WJ, Morley JE, Argiles J, Bales C, Baracos V, Guttridge D, Jatoi
22. Hunma S, Ramuth H, Miles-Chan JL, Schutz Y, Montani JP, Joonas A, Kalantar-Zadeh K, Lochs H, Mantovani G,, et al. Cachexia: a new
N, Dulloo AG. Body composition-derived BMI cut-offs for overweight definition. Clin Nutr 2008;27(6):793–9.
and obesity in Indians and Creoles of Mauritius: comparison with 42. Gonzalez MC, Pastore CA, Orlandi SP, Heymsfield SB. Obesity paradox
Caucasians. Int J Obes (Lond) 2016;40(12):1906–14. in cancer: new insights provided by body composition. Am J Clin Nutr
23. Marihart CL, Brunt AR, Geraci AA. The high price of obesity in nursing 2014;99(5):999–1005.
homes. Care Manag J 2015;16(1):14–19. 43. Park J, Ahmadi SF, Streja E, Molnar MZ, Flegal KM, Gillen D, Kovesdy
24. Batsis JA, Barre LK, Mackenzie TA, Pratt SI, Lopez-Jimenez F, Bartels CP, Kalantar-Zadeh K. Obesity paradox in end-stage kidney disease
SJ. Variation in the prevalence of sarcopenia and sarcopenic obesity in patients. Prog Cardiovasc Dis 2014;56(4):415–25.
older adults associated with different research definitions: dual-energy 44. Clark AL, Fonarow GC, Horwich TB. Obesity and the obesity paradox
x-ray absorptiometry data from the National Health and Nutrition in heart failure. Prog Cardiovasc Dis 2014;56(4):409–14.
Examination Survey 1999–2004. J Am Geriatr Soc 2013;61(6):974–80. 45. Soeters PB, Sobotka L. The pathophysiology underlying the obesity
25. McGregor RA, Cameron-Smith D, Poppitt SD. It is not just muscle mass: paradox. Nutrition 2012;28(6):613–15.
a review of muscle quality, composition and metabolism during ageing 46. Ard JD, Gower B, Hunter G, Ritchie CS, Roth DL, Goss A, Wingo BC,
as determinants of muscle function and mobility in later life. Longev Bodner EV, Brown CJ, Bryan D,, et al. Effects of calorie restriction in
Healthspan 2014;3(1):9. obese older adults: the CROSSROADS randomized controlled trial. J
26. Cava E, Yeat NC, Mittendorfer B. Preserving healthy muscle during Gerontol A Biol Sci Med Sci 2017;73(1):73–80.
weight loss. Adv Nutr 2017;8(3):511–19. 47. Messier SP, Mihalko SL, Legault C, Miller GD, Nicklas BJ, DeVita P,
27. Sakuma K, Aoi W, Yamaguchi A. Molecular mechanism of sarcopenia Beavers DP, Hunter DJ, Lyles MF, Eckstein F,, et al. Effects of intensive
and cachexia: recent research advances. Pflugers Arch 2017;469(5– diet and exercise on knee joint loads, inflammation, and clinical
6):573–91. outcomes among overweight and obese adults with knee osteoarthritis:
28. Muscaritoli M, Anker SD, Argiles J, Aversa Z, Bauer JM, Biolo G, Boirie the IDEA randomized clinical trial. JAMA 2013;310(12):1263–73.
Y, Bosaeus I, Cederholm T, Costelli P,, et al. Consensus definition of 48. Messier SP, Loeser RF, Miller GD, Morgan TM, Rejeski WJ, Sevick MA,
sarcopenia, cachexia and pre-cachexia: joint document elaborated by Ettinger WH Jr, Pahor M, Williamson JD. Exercise and dietary weight
Special Interest Groups (SIG) “Cachexia-anorexia in chronic wasting loss in overweight and obese older adults with knee osteoarthritis:
diseases” and “Nutrition in geriatrics”. Clin Nutr 2010;29(2):154–9. the Arthritis, Diet, and Activity Promotion Trial. Arthritis Rheum
29. Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS. Age and 2004;50(5):1501–10.
aerobic exercise training effects on whole body and muscle protein 49. Porter Starr KN, Pieper CR, Orenduff M, McDonald SR, McClure
metabolism. Am J Physiol Endocrinol Metab 2004;286(1):E92–101. LB, Zhou R, Payne ME, Bales CW. Improved function with enhanced
30. Melton LJ 3rd, Khosla S, Crowson CS, O’Connor MK, O’Fallon protein intake per meal: a pilot study of weight reduction in frail, obese
WM, Riggs BL. Epidemiology of sarcopenia. J Am Geriatr Soc older adults. J Gerontol A Biol Sci Med Sci 2016;71(10):1369–75.
2000;48(6):625–30. 50. Bales C, Porter Starr K, Orenduff M, McDonald S, Molnar K, Jarman
31. Costamagna D, Costelli P, Sampaolesi M, Penna F. Role of A, Onyenwoke A, Mulder H, Payne ME, Pieper CR. Influence of
inflammation in muscle homeostasis and myogenesis. Mediators protein intake, race, and age on responses to a weight reduction
Inflamm 2015; 2015:805172. intervention in obese women. Curr Dev Nutr 2017;1(5):e000703. DOI:
32. Fearon K, Evans WJ, Anker SD. Myopenia—a new universal term for https://doi.org/10.3945/cdn.117.000703.
muscle wasting. J Cachexia Sarcopenia Muscle 2011;2(1):1–3. 51. Backx EM, Tieland M, Borgonjen-van den Berg KJ, Claessen PR, van
33. Jensen MD, Ryan DH, Apovian CM, Ard JD, Comuzzie AG, Donato Loon LJ, de Groot LC. Protein intake and lean body mass preservation
KA, Hu FB, Hubbard VS, Jakicic JM, Kushner RF,, et al. 2013 during energy intake restriction in overweight older adults. Int J Obes
AHA/ACC/TOS guideline for the management of overweight (Lond) 2016;40(2):299–304.
and obesity in adults: a report of the American College of 52. Brown M, Sinacore DR, Binder EF, Kohrt WM. Physical and
Cardiology/American Heart Association Task Force on Practice performance measures for the identification of mild to moderate frailty.
Guidelines and The Obesity Society. J Am Coll Cardiol 2014;63(25 Pt J Gerontol A Biol Sci Med Sci 2000;55(6):M350–5.
B):2985–3023. 53. McConnell S, Kolopack P, Davis AM. The Western Ontario and
34. Tzankoff SP, Norris AH. Effect of muscle mass decrease on age- McMaster Universities Osteoarthritis Index (WOMAC): a review of its
related BMR changes. J Appl Physiol Respir Environ Exerc Physiol utility and measurement properties. Arthritis Rheum 2001;45(5):453–
1977;43(6):1001–6. 61.
35. Elia M, Ritz P, Stubbs RJ. Total energy expenditure in the elderly. Eur J 54. Weijs PJ, Wolfe RR. Exploration of the protein requirement during
Clin Nutr 2000;54(Suppl 3):S92–103. weight loss in obese older adults. Clin Nutr 2016;35(2):394–8.
36. Villareal DT, Apovian CM, Kushner RF, Klein S. Obesity in older 55. Wolfe RR, Cifelli AM, Kostas G, Kim IY. Optimizing protein intake
adults: technical review and position statement of the American Society in adults: interpretation and application of the recommended dietary
for Nutrition and NAASO, The Obesity Society. Am J Clin Nutr allowance compared with the acceptable macronutrient distribution
2005;82(5):923–34. range. Adv Nutr 2017;8(2):266–75.
37. Ten Haaf T, Verreijen AM, Memelink RG, Tieland M, Weijs PJ. 56. Houston DK, Nicklas BJ, Ding J, Harris TB, Tylavsky FA, Newman
Reduction in energy expenditure during weight loss is higher than AB, Lee JS, Sahyoun NR, Visser M, Kritchevsky SB,, et al. Dietary
predicted based on fat free mass and fat mass in older adults. Clin Nutr protein intake is associated with lean mass change in older, community-
2016. https://doi.org/10.1016/j.clnu.2016.12.014. dwelling adults: the Health, Aging, and Body Composition (Health
38. Weinheimer EM, Sands LP, Campbell WW. A systematic review of the ABC) study. Am J Clin Nutr 2008;87(1):150–5.
separate and combined effects of energy restriction and exercise on fat- 57. Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM. Increased
free mass in middle-aged and older adults: implications for sarcopenic consumption of dairy foods and protein during diet- and exercise-
obesity. Nutr Rev 2010;68(7):375–88. induced weight loss promotes fat mass loss and lean mass
39. Kalyani RR, Metter EJ, Ramachandran R, Chia CW, Saudek CD, gain in overweight and obese premenopausal women. J Nutr
Ferrucci L. Glucose and insulin measurements from the oral glucose 2011;141(9):1626–34.
tolerance test and relationship to muscle mass. J Gerontol A Biol Sci 58. Sahni S, Mangano KM, Hannan MT, Kiel DP, McLean RR. Higher
Med Sci 2012;67(1):74–81. protein intake is associated with higher lean mass and quadriceps
40. Soltani S, Hunter GR, Kazemi A, Shab-Bidar S. The effects of weight muscle strength in adult men and women. J Nutr 2015;145(7):1569–
loss approaches on bone mineral density in adults: a systematic review 75.

158 Bales and Porter Starr


Downloaded from https://academic.oup.com/advances/article-abstract/9/2/151/4969261
by guest
on 29 April 2018
59. McLean RR, Mangano KM, Hannan MT, Kiel DP, Sahni S. Dietary 72. Jesudason DR, Pedersen E, Clifton PM. Weight-loss diets in people
protein intake is protective against loss of grip strength among older with type 2 diabetes and renal disease: a randomized controlled trial
adults in the Framingham Offspring Cohort. J Gerontol A Biol Sci Med of the effect of different dietary protein amounts. Am J Clin Nutr
Sci 2016;71(3):356–61. 2013;98(2):494–501.
60. Bradlee ML, Mustafa J, Singer MR, Moore LL. High-protein foods and 73. Mojtahedi MC, Thorpe MP, Karampinos DC, Johnson CL, Layman
physical activity protect against age-related muscle loss and functional DK, Georgiadis JG, Evans EM. The effects of a higher protein
decline. J Gerontol A Biol Sci Med Sci 2017;73(1):88–94. intake during energy restriction on changes in body composition and
61. Symons TB, Schutzler SE, Cocke TL, Chinkes DL, Wolfe RR, Paddon- physical function in older women. J Gerontol A Biol Sci Med Sci
Jones D. Aging does not impair the anabolic response to a protein-rich 2011;66(11):1218–25.
meal. Am J Clin Nutr 2007;86(2):451–6. 74. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer
62. Pennings B, Groen B, de Lange A, Gijsen AP, Zorenc AH, Senden JM, DG, Scherr PA, Wallace RB. A short physical performance battery
van Loon LJ. Amino acid absorption and subsequent muscle protein assessing lower extremity function: association with self-reported
accretion following graded intakes of whey protein in elderly men. Am disability and prediction of mortality and nursing home admission. J
J Physiol Endocrinol Metab 2012;302(8):E992–9. Gerontol 1994;49(2):M85–94.
63. Symons TB, Sheffield-Moore M, Wolfe RR, Paddon-Jones D. A 75. Houston DK, Tooze JA, Hausman DB, Johnson MA, Nicklas BJ, Miller
moderate serving of high-quality protein maximally stimulates skeletal ME, Neiberg RH, Marsh AP, Newman AB, Blair SN,, et al. Change in
muscle protein synthesis in young and elderly subjects. J Am Diet Assoc 25-hydroxyvitamin D and physical performance in older adults. J
2009;109(9):1582–6. Gerontol A Biol Sci Med Sci 2011;66A(4):430–6.
64. Casperson SL, Sheffield-Moore M, Hewlings SJ, Paddon-Jones D. 76. Cipriani C, Pepe J, Piemonte S, Colangelo L, Cilli M, Minisola S.
Leucine supplementation chronically improves muscle protein Vitamin D and its relationship with obesity and muscle. Int J Endocrinol
synthesis in older adults consuming the RDA for protein. Clin Nutr 2014;2014:841248.
2012;31(4):512–19. 77. Verreijen AM, Verlaan S, Engberink MF, Swinkels S, de Vogel-van
65. Koopman R, Verdijk L, Manders RJF, Gijsen AP, Gorselink M, Pijpers den Bosch J, Weijs PJ. A high whey protein-, leucine-, and vitamin
E, Wagenmakers AJ, van Loon LJ. Co-ingestion of protein and leucine D-enriched supplement preserves muscle mass during intentional
stimulates muscle protein synthesis rates to the same extent in young weight loss in obese older adults: a double-blind randomized controlled
and elderly lean men. Am J Clin Nutr 2006;84(3):623–32. trial. Am J Clin Nutr 2015;101(2):279–86.
66. Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR. 78. Mason C, Tapsoba JD, Duggan C, Imayama I, Wang CY, Korde L,
Essential amino acids are primarily responsible for the amino acid McTiernan A. Effects of vitamin D3 supplementation on lean mass,
stimulation of muscle protein anabolism in healthy elderly adults. Am J muscle strength, and bone mineral density during weight loss: a
Clin Nutr 2003;78(2):250–8. double-blind randomized controlled trial. J Am Geriatr Soc 2016;64(4):
67. Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford 769–78.
AP, Casperson SL, Jiang J, Chinkes DL, Urban RJ. Amino acid 79. van Dronkelaar C, van Velzen A, Abdelrazek M, van der Steen A, Weijs
supplementation increases lean body mass, basal muscle protein PJM, Tieland M. Minerals and sarcopenia; the role of calcium, iron,
synthesis, and insulin-like growth factor-I expression in older women. magnesium, phosphorus, potassium, selenium, sodium, and zinc on
J Clin Endocrinol Metab 2009;94(5):1630–7. muscle mass, muscle strength, and physical performance in older adults:
68. Phillips SM, Tang JE, Moore DR. The role of milk- and soy-based a systematic review. J Am Med Dir Assoc 2018;19(1):6–11.
protein in support of muscle protein synthesis and muscle protein 80. Gonnelli S, Caffarelli C, Nuti R. Obesity and fracture risk. Clin Cases
accretion in young and elderly persons. J Am Coll Nutr 2009;28(4):343– Miner Bone Metab 2014;11(1):9–14.
54. 81. Von Thun NL, Sukumar D, Heymsfield SB, Shapses SA. Does bone loss
69. Bohe J, Low JF, Wolfe RR, Rennie MJ. Latency and duration of begin after weight loss ends? Results 2 years after weight loss or regain
stimulation of human muscle protein synthesis during continuous in postmenopausal women. Menopause 2014;21(5):501–8.
infusion of amino acids. J Physiol 2001;532(Pt 2):575–9. 82. Haywood CJ, Prendergast LA, Purcell K, Le Fevre L, Lim WK, Galea M,
70. Sakuma K, Yamaguchi A. Molecular mechanisms in aging and current Proietto J. Very low calorie diets for weight loss in obese older adults—a
strategies to counteract sarcopenia. Curr Aging Sci 2010;3(2):90– randomized trial. J Gerontol A Biol Sci Med Sci 2017;73(1):59–65.
101. 83. Villareal DT, Kotyk JJ, Armamento-Villareal RC, Kenguva V, Seaman P,
71. Beasley JM, LaCroix AZ, Neuhouser ML, Huang Y, Tinker L, Woods Shahar A, Wald MJ, Kleerekoper M, Fontana L. Reduced bone mineral
N, Michael Y, Curb JD, Prentice RL. Protein intake and incident frailty density is not associated with significantly reduced bone quality in
in the Women’s Health Initiative observational study. J Am Geriatr Soc men and women practicing long-term calorie restriction with adequate
2010;58(6):1063–71. nutrition. Aging Cell 2011;10(1):96–102.

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