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Preserving Healthy Muscle during Weight Loss

Article in Advances in Nutrition · May 2017

DOI: 10.3945/an.116.014506

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 REVIEW FROM ASN EB 2016 SYMPOSIUM

Preserving Healthy Muscle during Weight Loss1–3

Edda Cava, Nai Chien Yeat, and Bettina Mittendorfer*

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Center for Human Nutrition, Washington University School of Medicine, St. Louis, MO

ABSTRACT

Weight loss is the cornerstone of therapy for people with obesity because it can ameliorate or completely resolve the metabolic risk factors for
diabetes, coronary artery disease, and obesity-associated cancers. The potential health benefits of diet-induced weight loss are thought to be
compromised by the weight-loss–associated loss of lean body mass, which could increase the risk of sarcopenia (low muscle mass and impaired
muscle function). The objective of this review is to provide an overview of what is known about weight-loss–induced muscle loss and its
implications for overall physical function (e.g., ability to lift items, walk, and climb stairs). The currently available data in the literature show the
following: 1) compared with persons with normal weight, those with obesity have more muscle mass but poor muscle quality; 2) diet-induced
weight loss reduces muscle mass without adversely affecting muscle strength; 3) weight loss improves global physical function, most likely
because of reduced fat mass; 4) high protein intake helps preserve lean body and muscle mass during weight loss but does not improve muscle
strength and could have adverse effects on metabolic function; 5) both endurance- and resistance-type exercise help preserve muscle mass
during weight loss, and resistance-type exercise also improves muscle strength. We therefore conclude that weight-loss therapy, including a
hypocaloric diet with adequate (but not excessive) protein intake and increased physical activity (particularly resistance-type exercise), should be
promoted to maintain muscle mass and improve muscle strength and physical function in persons with obesity. Adv Nutr 2017;8:511–9.

Keywords: sarcopenia, dynapenia, weight loss, lifestyle therapy, muscle quality

Introduction muscle composition (e.g., deposition of noncontractile mate-

Obesity is associated with cardiometabolic diseases rial, such as lipids and connective tissue) and neuromuscular
(e.g., diabetes and coronary artery disease) (1–3) and certain adaptations to regular use or disuse that affect the ability of
types of cancer (e.g., colon) (4–6), and diet-induced weight muscle to generate force (19–21). Moreover, both weight
loss can ameliorate or completely resolve the metabolic risk loss and weight gain are accompanied by corresponding
factors (e.g., insulin resistance, dyslipidemia, increased blood changes in both body fat and fat-free (including muscle)
pressure) for these conditions (1–3, 5–8). The potential health mass (22–25). Accordingly, persons with obesity have more
benefits of diet-induced weight loss could be compromised by total fat-free and muscle mass than those with normal weight
the weight-loss–associated loss of lean body (including mus- (26–28). This review will focus first on what is known about
cle) mass (9, 10), which could increase the risk of sarcopenia the effects of obesity on muscle quality and function and sub-
(defined as low muscle mass and impaired muscle function) sequently discuss the effects of weight loss on muscle mass,
(10–12), especially in vulnerable populations, such as post- quality, and function and potential therapeutic strategies to
menopausal women and older adults (10, 13–18). In the gen- improve not only muscle mass but also muscle function in
eral population, muscle mass is a poor predictor of muscle persons with obesity. Articles to address these key questions
strength (19–21), because of interindividual differences in were selected from a thorough literature search in PubMed
intended to be inclusive of all relevant work in the area.
1
This article is a review from the symposium "Architecture of Healthy Muscles: The Interplay Note that, for simplicity, we refer to both fat-free and lean
between Exercise and Nutrition on Muscle Metabolism” held 5 April 2016 at the American body mass as fat-free mass throughout the article.
Society for Nutrition Scientific Sessions and Annual Meeting at Experimental Biology 2016
in San Diego, CA.
2
The authors received salary support from NIH grants DK 94483, DK 56341 (Washington
University School of Medicine Nutrition and Obesity Research Center), and UL1 TR000448 Current Status of Knowledge
(Washington University School of Medicine Clinical Translational Science Award); the Atkins Effect of obesity on muscle quality and muscle
Obesity Award; and the European Society for Parenteral and Enteral Nutrition while function
working on this manuscript.
3
Author disclosures: E Cava, NC Yeat, and B Mittendorfer, no conflicts of interest. Few studies have evaluated muscle mass, quality, and func-
*To whom correspondence should be addressed. E-mail: [email protected]. tion in people with obesity, but they consistently show that

ã2017 American Society for Nutrition. Adv Nutr 2017;8:511–9; doi:10.3945/an.116.014506. 511
obesity is associated with poor muscle quality, which ad- (as a proxy for limb muscle mass) by using whole-body
versely affects muscle function (27–30). Lafortuna et al. DXA (47, 52, 54, 56, 65, 66). The reductions in muscle
(27) found an inverse relation between adiposity and muscle mass in young and old men and women with obesity after
lipid content (assessed by X-ray attenuation) in middle-aged diet-induced weight-loss of 8–10% were ;2–10% (47, 52–
and older men and women. Choi et al. (28) found that older 56, 59, 62–66). Such changes are significant but most likely
adults with obesity had ;20% more thigh muscle mass and reflect a new (post–weight loss) muscle mass that is consistent
;2 times more muscle lipid content (assessed in vivo as ul- with the new, reduced body weight rather than a diet-induced
trasound echo intensity) than older adults with normal “muscle deficit” because of the greater initial muscle mass
weight (28). They also found that obesity was associated in persons with obesity than in those with normal weight
with reduced ex vivo single-myofiber function (peak Ca2+- (24–28).
activated force) and in vivo muscle function (peak torque) Bariatric surgery, which results in rapid and massive
(28). Furthermore, they found an inverse relation between weight loss (>20% of total body weight), does not seem to
the average number of lipid droplets in myofibers and accelerate the loss of fat-free mass relative to total body or

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single-fiber unloaded shortening velocity, maximal velocity, fat mass loss (67–72). Most studies that evaluated the effect
and specific power and an inverse relation between muscle of bariatric surgery–induced weight loss on body composi-
lipid content (assessed in vivo as ultrasound echo intensity) tion found that neither restrictive nor malabsorptive proce-
and single-fiber specific force (28). Large epidemiologic stud- dures resulted in excessive amounts of fat-free relative to fat
ies have also shown an inverse association between muscle mass loss 1–2 y after surgery (67–72). The average contribu-
lipid content (assessed by X-ray attenuation) and maximum tion of fat-free mass to total weight loss was <30%, and the
voluntary strength (29) and walking speed (30). Reduced relative contribution of fat-free mass to total body weight af-
muscle strength and power are key predictors of serious ad- ter weight loss was either not different or even greater than
verse outcomes in older adults, including the inability to carry in sex-, age-, and BMI-matched control subjects (67–72).
out activities of daily living (31), mobility disability (32–34), Only 1 study reported a contribution of >35% of fat-free
falls (;20% increase in incidence rate for each ;15% de- mass to total body weight loss 1–2 y after sleeve gastrectomy
crease in lower leg strength), hip fracture (35–39), and mor- and Roux-en-Y gastric bypass surgery (73).
tality (;4% increase for every 1-kg decrease in grip strength) Only 2 studies evaluated the effect of bariatric surgery on
(40, 41). Indeed, obesity in older adults is associated with surrogate measures of muscle mass (72, 74). One (72) eval-
poor physical function, assessed by using the Modified Phys- uated changes in appendicular lean mass after sleeve gastrec-
ical Performance Test, which includes activities such as climb- tomy and Roux-en-Y gastric bypass surgery but did not
ing stairs, rising from a chair, lifting a book onto a shelf, and include a diet-induced weight-loss or weight-maintenance
walking speed (42), and an increased risk of falls (as much as control group. Appendicular lean body mass loss was highly
in people with vision problems or a stroke) (43). Improving variable: approximately two-thirds of the subjects lost <15%
muscle quality, rather than preserving or increasing muscle and one-third lost >15% of their appendicular lean mass 1 y
mass, should therefore be the primary focus of therapeutic after surgery in that study (72). The other study (74) evalu-
strategies for people with obesity. ated vastus medialis thickness after matched weight loss
achieved by either a hypocaloric diet or gastric banding
Effect of diet-induced weight loss on muscle mass in and found a greater reduction in vastus medialis thickness
persons with obesity in the bariatric surgery group than in the diet-induced
Weight loss, achieved through a calorie-reduced diet, de- weight-loss group (;3% compared with 0.5%/y). The
creases both fat and fat-free (or lean body) mass (44–46). mechanism responsible for the difference in muscle loss in
In persons with normal weight, the contribution of fat- that study (74) is unclear because gastric banding is a purely
free mass loss often exceeds 35% of total weight loss (47, restrictive procedure (i.e., it results in weight loss entirely be-
48), and weight regain promotes relatively more fat gain cause of reduced dietary energy intake). Accordingly, the ef-
(49). In persons who are overweight or obese, fat-free mass fect of bariatric surgery on muscle mass remains unclear.
contributes only ;20–30% to total weight loss (48, 50–59),
and weight regain does not prevent fat-free mass regain Mechanisms responsible for loss of muscle mass
(49). Men tend to lose more fat-free mass than women, espe- during diet-induced weight-loss–protein synthesis
cially shortly after the initiation of weight loss (60, 61), prob- versus breakdown
ably because they are leaner than women (26). Diet-induced The mechanisms responsible for the weight-loss–induced
weight loss in those with obesity therefore results in a more decrease in muscle mass (reduced muscle protein synthesis,
favorable fat-free mass to fat mass ratio despite loss of lean increased breakdown, or both) have not been extensively
mass, and weight cycling (yo-yo effect) has no adverse effect studied. Studies that evaluated the effect of short-term
on body composition in persons with obesity (49). (14–21 d) calorie restriction (;30–40% energy deficit/d)
The effect of diet-induced weight loss on muscle mass has on the rate of muscle protein synthesis in young and
been evaluated by measuring changes in muscle volume by middle-aged men and women who were overweight and
using MRI or computed tomography (53, 55, 59, 62–64) obese found that calorie restriction decreases the postprandial
or by measuring changes in appendicular lean body mass rate of muscle protein synthesis and decreases or does not

512 Symposium
change the basal rate of muscle protein synthesis (75–77). the loss was ;70% greater in the diet-alone group
Prolonged moderate calorie restriction and 5–10% weight (25.2%) compared with the diet-plus-exercise (23.0%)
loss, on the other hand, increased the rate of muscle protein group. Together, these results suggest that resistance-type
synthesis (78, 79). The loss of muscle mass during prolonged exercise is an effective strategy to attenuate or even
moderate calorie restriction is therefore mediated by in- prevent the weight-loss–induced loss of muscle mass during
creased muscle proteolysis rather than suppressed muscle weight loss, whereas the effects of endurance-type exercise
protein synthesis. on muscle mass during weight loss are uncertain. Nicklas
et al. (93) evaluated the effect of adding calorie restriction
Strategies to prevent the weight-loss–induced loss of to a resistance exercise program (3 d/wk) in older men and
muscle mass women with obesity and found that it prevented the
Regular physical activity, especially resistance-type exercise exercise-induced increase in thigh muscle volume but did
training, and high protein intake (1.25–1.5 times the RDA not decrease it compared with baseline values. These
for sedentary persons and >1.5 times the RDA for those findings confirm the opposing actions of a hypocaloric diet

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who exercise) are recommended for persons with obesity and resistance exercise training on muscle mass.
who undergo weight-loss therapy to limit the loss of muscle
mass (80–82), because dietary amino acids, insulin, and Effect of high-protein intake on lean body and muscle
contractile activity are the major regulators of muscle pro- mass during diet-induced weight loss. During energy bal-
tein synthesis and breakdown (83). Amino acids and dietary ance or dietary energy excess, inadequate protein intake
protein stimulate muscle protein synthesis in a dose- (i.e., less than the RDA of 0.8 g $ kg21 $ d21) results in loss
dependent manner # ;20 g protein/meal (84, 85). Insulin of total body fat-free and muscle mass (;0.220.5%/wk)
is a potent inhibitor of muscle protein breakdown and max- (23, 94–96). During negative energy balance induced
imally suppresses muscle protein breakdown at plasma insu- by a calorie-reduced diet, inadequate protein intake
lin concentrations of 15–30 mU/mL (86–89). Exercise (both augments the weight-loss–induced loss of lean body mass
resistance and endurance type) improves insulin sensitivity (97, 98). However, adding protein to a diet that already
(90, 91) and stimulates muscle protein synthesis (92). The contains the RDA of protein has no beneficial effect on total
effects of increased physical activity, exercise training, and body fat-free and muscle mass during weight maintenance
increased protein intake during weight-loss therapy on mus- or weight gain (23, 99, 100). Whether increasing protein
cle mass and muscle function are summarized in the follow- intake during weight loss can limit the weight-loss–induced
ing sections. loss of fat-free mass is unclear because of conflicting results
reported in the literature (54, 56, 96, 98, 101–108). The
Effects of exercise training or increased physical activity reasons for the discrepancy in results in these studies (54, 56,
on muscle mass during diet-induced weight loss. Several 96, 98, 101–108) are not readily apparent but could be related
investigators found that a progressive resistance exercise to differences in baseline protein intake, diet composition,
training program in conjunction with a hypocaloric diet at- duration of the intervention, and the small effect of extra
tenuated the weight-loss–associated loss of muscle mass in protein on fat-free mass, which may make it difficult to
middle-aged and older men and women (55, 65, 66). The detect the difference in studies with small sample sizes. For
effect of endurance-type exercise training on muscle mass example, Backx et al. (56) found no effect of protein
during weight-loss therapy, however, is less clear (53, 59, supplementation on fat-free mass loss during weight loss in
62–64). In middle-aged and older men and women with older men and women who already consumed the RDA of
obesity, both a hypocaloric diet alone and a hypocaloric protein with their diet, whereas Schollenberger et al. (98)
diet combined with $300 min/wk of moderate-intensity found that fat-free mass loss after Roux-en-Y gastric bypass
aerobic exercise decreased thigh muscle cross-sectional surgery was attenuated in subjects who received protein
area, but the decrease in the diet-plus-exercise group was supplementation compared with those who did not and
only approximately half that in the diet-only group (63). consumed less than the RDA of protein. The results from
Two other studies found that daily brisk walking for ;1 h the most recent systematic review and meta-analysis (109)
or vigorous endurance-type exercise for ;1 h for 6 d/wk support a very small but significant beneficial effect (400–
preserved muscle mass, whereas weight loss achieved by 800 g of lean mass preservation) of high protein intake on
consuming a hypocaloric diet decreased muscle mass in fat-free mass during weight-loss therapy.
middle-aged and older men and women (53, 59). Others The effect of varying protein intake on muscle mass dur-
(62, 64), however, found that the addition of 35–45 min of ing diet-induced weight loss has not been adequately stud-
aerobic exercise (moderate-intensity walking) 3–5 times/wk ied. We are aware of only one study that evaluated the
in obese older men and women led to decreases in thigh effect of increased protein intake during weight-loss therapy
and trunk muscle cross-sectional areas similar to diet alone. on muscle mass in older adults with obesity who lost weight
Failure to detect a beneficial effect of exercise on muscle by consuming a hypocaloric diet and were engaged in a re-
mass in $1 of these studies (64) may have been due to the sistance exercise training program (54). It found that sub-
small sample size and/or large interindividual variability jects who added a whey protein–, leucine–, and vitamin
in the response, which reduces statistical power, because D–enriched supplement compared with subjects who added

Weight loss and muscle mass and function 513

TABLE 1 Effects of obesity and weight loss on muscle mass, muscle strength, and global elderly patients (118). Esmarck et al.
physical function1 (119) evaluated the effect of protein
Weight loss supplementation in older men who
CR with increased muscle activity participated in a 12-wk resistance ex-
CR + Endurance exercise or Resistance ercise training program and were
Obesity CR HP PA exercise asked to consume a protein supple-
Muscle mass O . L YY Y Y 4 ment either immediately after or 2 h
Muscle strength2 O,L 4 4 4 [
Global physical O,L [ [ [[ [[
after exercise. They found that the
function cross-sectional area of the quadriceps
1
Double arrows indicate greater magnitude of effect than single arrow. CR, calorie restriction; HP, high protein; L,
femoris and its mean myofiber area in-
lean; O, obese; PA, physical activity. Y, decrease; [, increase; 4, no change. creased in subjects who consumed the
2
Intrinsic strength per unit of muscle mass or muscle fiber. supplement immediately after exer-
cise but not in those who consumed

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it 2 h after the exercise (119). The ex-
an isocaloric control drink to their diet (total protein intake: ercise training sessions were performed between 800 and
1.1 compared with 0.85 g protein $ kg21 $ d21) preserved 1000 in the morning, so that subjects consumed the supple-
appendicular muscle mass during weight loss. ment either several hours after breakfast (immediately after
As important as total daily protein intake could be the exercise) or shortly before lunch (2 h after exercise) (119). It
distribution of dietary protein intake over the course of is therefore possible that the difference in the effect was due
the day, because there appears to be a refractory period to the timing of the protein supplement relative to meal in-
during which muscle protein synthesis, once stimulated take rather than the timing relative to the exercise session.
by amino acids, cannot be stimulated again (“muscle-full” The effect of protein intake distribution on muscle protein
phenomenon) (110). Accordingly, 2 studies conducted in synthesis or muscle mass during weight-loss therapy has,
healthy young and middle-aged men and women (111, to our knowledge, not been studied.
112) reported a greater overall muscle protein synthesis Together, these results suggest that increased protein in-
rate throughout the day when protein intake was evenly dis- take, if distributed evenly throughout the day, may prevent
tributed throughout the day than with skewed protein intake the loss of muscle mass during weight-loss therapy. How-
(most of the protein consumed at dinner). The results ever, the additional protein may have adverse effects on
from a recent retrospective analysis in a subset of subjects glucose metabolism. Smith et al. (106) showed that pro-
who participated in the NuAge study (Quebec Longitudinal tein supplementation of a hypocaloric diet eliminates the
Study on Nutrition as a Determinant of Successful Aging) weight-loss–induced improvement in muscle insulin sensitiv-
also suggest that a more even distribution of protein intake ity (assessed by using the hyperinsulinemic-euglycemic clamp
across meals is associated with more appendicular lean body procedure), even though weight loss was the same (10%) in
mass than is a skewed protein intake (least for breakfast, both the high-protein and standard-protein diet groups. In
most at dinner) in older adults (113). Long-term prospective addition, data from small cross-sectional (120, 121) and large
randomized controlled studies evaluating the effect of even epidemiologic (122–126) studies suggest that high protein in-
compared with skewed protein intakes on muscle mass (or take is involved in the pathogenesis of insulin resistance and
surrogate measures of muscle mass) are missing. The results type 2 diabetes.
from studies that compared the effect of even and skewed
protein intakes on whole-body nitrogen retention and pro- Effect of diet-induced weight loss on muscle quality,
tein balance are equivocal and often contradict the acute ef- muscle strength, and physical function
fects of even compared with skewed protein intake on Diet-induced weight loss reduces muscle lipid content (as-
muscle protein synthesis (111, 112) and the results from ret- sessed by X-ray attenuation or MRI) (52, 62, 63, 74) and
rospective analysis of the NuAge study data (113). Two ran- does not affect (55, 65, 93), or slightly decreases (48, 52,
domized clinical trials in healthy middle-aged and older 56), leg muscle strength. Grip strength and global measures
adults found no benefit of even, compared with skewed, of physical function, such as balance, walking speed, or
protein intake on whole-body protein balance and muscle climbing stairs, improve after weight loss (52, 54–56, 93,
protein synthesis during weight maintenance (114) and 115, 127). The improvements in physical function after
fat-free mass retention during weight-loss therapy (115), diet-induced weight loss are most likely due to the loss of ex-
even though total protein intake was greater in the even- cess total body fat mass (128), which can interfere with
protein-intake group (1.2 g $ kg21 $ d21) than in the range of motion, gait, etc. Weight loss induced by increasing
skewed-protein-intake group (0.8 g $ kg21 $ d21) (115). energy expenditure through exercise (endurance or com-
Others found that protein pulse feeding (ingesting 80% of bined endurance and resistance type) improves muscle
daily intake in one meal), compared with evenly distributed strength compared with diet-induced weight loss but does
protein intake, increased whole-body nitrogen retention in not improve strength compared with weight maintenance
healthy elderly (116) [but not young (117)] women and in- and does not improve physical function more than
creased fat-free mass retention in malnourished hospitalized diet-induced weight loss (53, 55). Combined diet- and

514 Symposium
exercise-induced weight loss, on the other hand, results in muscle strength; 4) high protein intake helps preserve lean
greater improvements in physical function than weight body and muscle mass but does not improve muscle
loss through diet alone or exercise alone (53, 55). Most studies strength and could have adverse effects on metabolic func-
that evaluated the effect of increasing protein intake during tion. We therefore conclude that weight-loss therapy,
weight loss on muscle strength and physical function did including a hypocaloric diet with adequate (but not exces-
not find a beneficial effect of high protein intake on leg muscle sive) protein intake, and physical activity, particularly re-
strength or physical function in young and old and sedentary sistance exercise–type training, should be promoted to
or physically active adults (54, 56, 98, 107). We are aware of maintain muscle mass and improve muscle strength and
only one study (115) that found a small, but nonetheless sig- physical function in persons with obesity.
nificantly greater, increase in physical function (assessed by us-
ing the Short Physical Performance Battery) in older obese Acknowledgments
adults who lost ;10% of their body weight and consumed All authors read and approved the final manuscript.
1.2 g protein $ kg body weight21 $ d21 and $30 g protein/meal

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than subjects in the control group who were instructed to con-
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