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Protein Applications in
Sports Nutrition—Part II:
Timing and Protein
Patterns, Fat-Free Mass
Accretion, and Fat Loss
Kurt A. Escobar, MA, CSCS,
1
Trisha A. McLain, MS,
1
and Chad M. Kerksick, PhD, CSCS*D, ATC,
NSCA-CPT*D
2
1
Department of Health, Exercise and Sports Sciences, University of New Mexico, Albuquerque, New Mexico; and
2
Department of Exercise Science, School of Sport, Recreation and Exercise Sciences, Lindenwood University,
St. Charles, Missouri
ABSTRACT
A NUMBER OF KEY CONSIDERA-
TIONS EXIST REGARDING PRO-
TEIN, INCLUDING OVERT
REQUIREMENTS, QUALITY, AND
DOSING. IN ADDITION, ATHLETES
AND RESEARCHERS HAVE
CLOSELY EXAMINED THE IMPACT
OF PROTEIN AND NUTRIENT TIM-
INGONACUTEANDPROLONGED
ADAPTATIONS TO DIFFERENT
TYPES OF EXERCISE WITH MIXED
RESULTS. THE PATTERN OF MEAL
AND PROTEIN CONSUMPTION
SEEMS TO EXERT AN IMPACT ON
CHANGES RELATED TO HEALTH,
BODY COMPOSITION, AND MUS-
CLE PROTEIN SYNTHESIS. PRO-
TEIN IS A KEY NUTRIENT FOR
INDIVIDUALS LOOKING TO LOSE
WEIGHT, REDUCE THEIR BODY
FAT, AND IMPROVE THEIR
HEALTH.FINALLY,PROTEIN
INTAKE CONTINUES TO BE A KEY
VARIABLE FOR ATHLETES LOOK-
INGTOGAINSTRENGTH,
POWER, AND FAT-FREE MASS.
OVERVIEW
Within sports nutrition, pro-
tein, a key macronutrient,
continues to capture a great
deal of attention. For a number of
years, the notion that greater protein
was required by exercising individuals
was (and to some degree still is) a con-
troversial topic. As anecdotal and
empirical research began to accumu-
late to support its use, an appreciation
for the utility of protein began to
develop. In an attempt to further
enhance the known benefits of con-
suming adequate amounts of the mac-
ronutrients, researchers began to
explore nutritional strategies to further
heighten favorable changes within
exercising muscle by manipulating
the time when nutrients were provided
as well as different types of certain
macronutrients. Initial timing research
centered on carbohydrates. Several
years later, research became focused
on protein timing with recent investi-
gators exploring the potential impact
of altering the patterns of protein
meals to stimulate increases in muscle
protein synthesis (MPS) and promote
improvements in health and body
composition. Finally, the addition of
protein as part of a resistance training
program to further promote increases
in strength and fat-free mass (FFM)
continues to be one of the most pop-
ular applications of protein, particu-
larly with athletes and other sectors
of sports nutrition. In this light, the
role of protein as a part of a weight
loss program to better control appetite
and feelings of satiety as well as to
facilitate greater losses of body fat,
while better maintaining levels of
FFM continues to be seen as a greater
empirical support from the available
literature. The purpose of this brief
review is to discuss available literature
as it relates to topics such as protein
timing, patterns of protein consump-
tions, and alterations in protein intake
to facilitate adaptations related to
FFM accretion and fat mass loss.
TIMING AND PROTEIN PATTERNS
Protein timing continues to be a popu-
lar strategy to enhance observed
VOLUME 37 | NUMBER 3 | JUNE 2015 Copyrig ht ÓNational Strength and Conditioning Association
22
physiological adaptations to exercise.
For a deeper discussion on the topic,
reviews of varying viewpoints (4,30,52)
and books (7,29,53) have been written
regarding the concept, but it is impor-
tant to highlight that research exists
exploring all timing considerations
involving both aerobic and resistance
exercise in regards to carbohydrate and
protein. Currently, little research exists
examining the impact of timed protein
ingestion surrounding aerobic exercise
performance as the majority of this lit-
erature has involved resistance exer-
cise. Without question, the impact of
carbohydrate administration provided
before a bout of prolonged endurance
exercise holds great potential to
improve parameters of endurance per-
formance (15,62), but administration of
protein or amino acids before endur-
ance exercise is lacking in the literature.
On considering known patterns of sub-
strate utilization (carbohydrate and fat
breakdown in favor of protein and
amino acid breakdown during aerobic
exercise) and the particular problems
that can result from a digestive perspec-
tive with preaerobic exercise ingestion
of protein and amino acids, the lack of
literature is somewhat understood.
Ingestion of amino acids (as hydro-
lyzed protein) throughout a bout of
endurance exercise in conjunction
with carbohydrate delivery has been
shown to improve subsequent muscle
damage (e.g., creatine kinase) as well
as time to exhaustion performance
(50,51). Similarly, Miller et al. had 9
male runners complete 3 similar inves-
tigative trials involving a 2-hour run at
65% V
O
2
max. Blood samples were col-
lected in response to exercise and feed-
ing then measured for changes in
insulin, glucagon, epinephrine, norepi-
nephrine, growth hormone, testoster-
one, and cortisol. Protein and amino
acid ingestion resulted in significant in-
creases in glucagon, as well as signifi-
cant attenuations of free fatty acids and
amino acid levels (44). However, these
studies were not designed with the
intention to examine the true impact
of timing, thus the impact of protein
timing per say on these outcomes
remains somewhat undetermined. Pro-
tein or amino acid ingestion during the
postexercise time period was initially
shown by Zawadzki et al. (65), who
found that rates of glycogen resynthe-
sis are significantly greater when
compared with just ingestion of
carbohydrates. However, subsequent
research has indicated that this effect
is most evident when total ingestion of
carbohydrate is lower than what is ex-
pected considering the athlete’s activ-
ity level (12). Bolster et al. (9) had 5
endurance-trained male runners
(21.3 60.3 years; 179.1 61.7 cm;
70.6 60.1 kg; 70.6 60.1
mL$kg
21
$min
21
) complete a 75-
minute treadmill run at 70% V
O
2
peak
after ingesting diets of varying protein
content (low protein, equal to the
recommended daily allowance
[RDA]: 0.8 g/kg; moderate protein,
equal to 2.253the RDA: 1.8 g/kg; high
protein, equal to 4.53the RDA: 3.6
g/kg) for a 4-week period. MPS was
measured after the run, and signifi-
cantly greater rates of MPS were found
after each subsequent level of dietary
protein intake (high protein .moder-
ate protein .low protein), whereas no
difference was found between moder-
ate protein and low protein (p.0.05).
For years, the majority of focus was
put on consuming nutrients after
asingleboutofresistanceexercise
(4+ sets of 10 repetitions at 70–85%
1 repetition maximum [RM] with
2 minutes of rest between sets), and
this continues to remain popular.
However, in 2001, Tipton et al con-
cluded that consuming an identical
combination of carbohydrates (35 g)
and essential amino acids (6 g) imme-
diately before a single bout of resis-
tance training (10 sets of 8 leg press
repetitions at 80% 1RM and 8 sets of
8 leg extension repetitions at 80%
1RM) resulted in greater rates of
MPS than immediate postexercise
ingestion. Rest periods between sets
were 2 minutes, and the entire exercise
bout took ;45–50 minutes. Follow-up
studies by Fujita et al. and Tipton et al.
in 2007 refuted these original findings
resulting in the conclusion that neither
ingestion time point illustrates signifi-
cant superiority over the other, as both
can robustly stimulate maximal rates of
MPS (21,56,58).
An overwhelming majority of research
has explored the impact of ingesting
various combinations of nutrients after
a bout of resistance exercise. This
research consistently demonstrates
that ingestion of single doses (6–12 g)
of the essential amino acids alone or in
combination with carbohydrates max-
imally stimulates rates of MPS and im-
proves muscle protein balance
(10,11,57), particularly when ingestion
occurs immediately after or within 3
hours of completing a resistance exer-
cise bout. In summary, little dispute
arises regarding the ability of essential
amino acids with or without carbohy-
drate immediately after, 1, 2, or 3 hours
after exercise to maximally stimulate
increases in MPS (11,28,57–59).
Numerous studies are available that
have provided protein alone or in
combination with carbohydrate after
resistance training bouts over the
course of several weeks. Collectively,
results from these studies indicate that
providing a 15–40 g dose of high-
quality protein in conjunction with
heavy resistance training facilitates
improvements in strength, endurance,
power, and body composition
(17,23,34,49,63). Moreover, an excel-
lent meta-analysis by Cermak et al.
supports the notion that an increased
intake of protein is favorable toward
resistance training adaptations, such
as strength and FFM gains (13).
Although studies have provided nu-
trients after a workout bout and exam-
ined outcomes, very few studies have
been designed with the explicit purpose
to examine the impact of protein timing
on the adaptations made by several
weeks or months of resistance training.
In this respect, 2 recently published
well-constructed reviews by Aragon
and Schoenfeld (4,52) are available to
the interested reader that highlight
the impact of postexercise timing
of protein. Andersen et al. had partici-
pants consume isocaloric amounts of
Strength and Conditioning Journal | www.nsca-scj.com 23
carbohydrate or protein immediately
before and immediately after the last
set of resistance training over 14 weeks
and examined changes in performance
and muscle cross-sectional area. Supple-
ments were ingested first thing in the
morning on nonworkout days. Timed
ingestion of protein led to greater in-
creases in hypertrophy when compared
with timed ingestion of carbohydrate
(2). One year later, in 2006, Cribb and
Hayes published their findings that pro-
vided what seemed to be the strongest
evidence for protein timing. Over the
course of several weeks, 2 groups in-
gested identical amounts of protein, car-
bohydrate, and creatine (32 g protein,
34.4 g carbohydrate, 5.6 g creatine for
a 80-kg participant), but 1 group in-
gested the protein and carbohydrate
combination immediately before and
after their workouts. The other group
ingested the protein and carbohydrate
combination before breakfast and
shortly before going to bed on workout
and evening on workout days. In addi-
tion, all participants trained between
3 and 6 p.m. and approximately 1–2
hours passed between the completion
of their workout and their evening
meal (16). Both groups experienced
favorable increases in strength and lean
body mass (LBM), but when nutrients
were ingested at times closely sur-
rounding each training bout signifi-
cantly greater increases in LBM,
maximal strength and muscle cross-
sectional area were realized (16). In
2009, researchers used a very similar
study design using trained collegiate
athletes and reported no differences
in performance or body composition
between 2 groups of athletes ingesting
protein close to each workout and
identical amounts of nutrients in the
morning and evening of training
days (24). Conclusions from this work
highlight the impact of consuming
adequate amounts of protein on a daily
basis whereby the participants in the
second study were consuming higher
amounts of calories and protein. Thus,
it seems that overall protein intake may
be operating as a more powerful factor
when compared with timely con-
sumption, although timing closely
surrounding workouts does not hinder
training outcomes.
The pattern of protein consumption
has been increasingly investigated as
well and in many respects, can be
viewed as an extension of nutrient or
protein timing. Two published studies
from the same group of study subjects
revealed that in response to a single
bout of resistance exercise in healthy
subjects, an intermediate sized dose
(20 g) of whey protein isolate ingested
every 3 hours over a 12-hour study
window led to the greatest improve-
ments in the overall balance of protein
in the body and greater synthesis rates
of protein found in skeletal muscle
(6,45). From a health and fat loss per-
spective, Arciero et al. invoked a con-
trolled pattern of protein feeding with 3
daily 20-g doses of whey protein at
prescribed times to overweight study
participants and combined it with no
exercise, a resistance training program,
or a combination of different types of
exercise programs (high-intensity in-
tervals, resistance training, interval
sprint training, yoga, stretching or
Pilates). Both exercise programs
completed 4 workouts sessions per
week. Outside of the prescribed protein
feedings, all participants were in-
structed to follow their typical dietary
practices and not alter their caloric
intake or macronutrient distribution
of foods consumed in their daily diet.
The lack of a control group precluded
the ability to determine the actual
impact of protein feeding patterns,
but of greatest importance, all groups
lost significant amounts of weight and
fat mass (5).
FAT-FREE MASS
The combination of muscular loading
through resistance training and protein
feeding is known to instigate wide-
spread intramuscular changes that
result in the accretion of FFM
(13,48). Proteins are simultaneously
being synthesized and degraded pro-
viding the basis for skeletal muscle’s
plastic response to loading (i.e., resis-
tance training) (48). Protein ingestion
increases MPS and reduces rates of
muscle protein degradation seen in
response to resistance exercise facili-
tating a positive muscle protein
balance and setting the stage for the
accretion of muscle mass (14). For this
reason, supplementation with protein
is used during periods of resistance
training to optimize enhancements
in FFM. Over time, MPS stimulated
by protein ingestion results in protein
accretion and may lead to hypertro-
phy when coupled with resistance
training (47). Thus, increases in
LBM are the result of chronic resis-
tance training and provision of amino
acids and/or protein, which results
in a robust increase in net protein
balance (32).
In a study by Cribb et al. (2007), 10
recreational bodybuilders were given
a total dose of 1.5 g$kg
21
$d
21
consist-
ing of either whey isolate protein,
protein + carbohydrate or protein +
carbohydrate + creatine while partici-
pating in a high-intensity, 3-phase
resistance training program for 10
weeks (18). Subjects consumed the
prescribed supplement dose in 3 equal
servings (0.5 g$kg
21
$d
21
) throughout
the day (i.e., midmorning, posttraining,
and before sleep); total dietary intake
ranged from 1.6 to 2.3 g$kg
21
$d
21
.The
supplementation of whey isolate led to
an LBM increase of approximately 5 kg
at the end of the 10-week training
period. In another study, Cribb et al.
(17) investigated the effects of whey
as well as casein protein supplementa-
tion on FFM. Thirteen recreational
bodybuilders supplemented with either
1.5 g$kg
21
$d
21
of whey isolate or
casein protein for 10 weeks while
engaging in high-intensity resistance
training. The supplement dose was
divided into smaller equal servings
(i.e., breakfast, lunch, posttraining,
and dinner). Lean mass was signifi-
cantly greater over the 10-week train-
ing period in the whey isolate group,
with an LBM gain of 5 kg, whereas the
casein group also illustrated a near 1-kg
increase in LBM. Willoughby et al.
investigated the combined effects of
protein and amino acid supplementa-
tion after 10 weeks of heavy resistance
VOLUME 37 | NUMBER 3 | JUNE 2015
24
training. Ten untrained males con-
sumed a 14-g combination of whey
and casein protein along with 6 g of
amino acids, whereas 9 men were
given an isocaloric placebo beverage
of 40 g of dextrose. Ingestion occurred
1 hour before training and immediately
after training. Subjects consuming the
blend of protein and amino acids dis-
played significantly greater increases in
FFM (5.62 60.98 kg) versus the pla-
cebo group (2.7 61.31 kg), respec-
tively. Burke et al. (2001) reported
a significant 2.3-kg increase in LBM
in recreationally trained men after sup-
plementing with 1.2 g$kg
21
$d
21
of
whey protein (in 4 equal servings) dur-
ing 6 weeks of resistance training.
Finally, 2 studies published by Kerksick
et al. examined the impact of protein
supplementation on changes made
while resistance training over several
weeks. The first study published in
2006 reported that college-aged men
who consumed a 48-g blend of whey
and casein protein experienced signifi-
cant gains in LBM and strength while
after a 10-week split-body (2 upper-
body and 2 lower-body workouts per
week, 6–12RM) resistance training
program (34). In 2007, Kerksick et al.
(33) used the same resistance training
program over a 12-week time period
and supplemented 49 healthy men
and women with various combinations
of protein and found that all groups
experienced significant increases in
strength and LBM; however, no carbo-
hydrate placebo group was included in
this study, as researchers were examin-
ing the impact of various sources of
protein with and without the addition
of creatine monohydrate. An upper limit
of optimal protein intake to modulate
body composition changes, while resis-
tance training is currently unknown.
Although the majority of published
studies have used relative protein
prescriptions of 1.2–2.0 g$kg
21
$d
21
or
absolute individual protein doses rang-
ingfrom10to40gperdaydeliveredin
1–3doses,astudypublishedin2014by
Antonio et al. reported that participants
consuming a hypercaloric diet at a pro-
tein dose of 4.4 g$kg
21
$d
21
(.53the
RDA for protein) did not result in fat
mass gains and also promoted increases
in body mass and FFM (3). Although
more research is needed, these results
open the door for more research to
explore even higher intakes of protein
to examine what seems to be a unique
role for protein to favorably impact body
composition (Table 1).
Moreover, a meta-analysis by Cermak
et al. outlined the effects of 22 random-
ized controlled studies that included
680 subjects and reported that com-
pared with a placebo, protein supple-
mentation significantly augmented
FFM gain (+0.69 kg; p,0.001) and
strength (+13.5 kg, p,0.005) during
prolonged periods (12 65 weeks) of
resistance training in both younger and
older adults. These results provide
sound evidence that protein supple-
mentation, or adequate protein intake,
is required to maximize the physiolog-
ical adaptations made in response to
prolonged resistance training.
In summary, muscle protein accretion
in response to resistance exercise is the
result of successive periods of positive
muscle protein balance (23). Amino
acids found in protein represent the
primary effectors of skeletal muscle
protein metabolism through their abil-
ity to stimulate increased rates of MPS,
suppress breakdown, and promote
a net positive protein balance (14).
The provision of essential amino acids
favorably influences muscle protein
balance over a 24-hour period by elic-
iting changes in muscle protein turn-
over (49). Protein supplementation
(whey, casein, and amino acids in par-
ticular) impacts the regulation of mus-
cle mass (25) stemming from the
resultant net positive protein balance
(14,35). Finally and most convincingly,
LBM gains occur in trained and
untrained young populations and
older adults after periods of concurrent
resistance training and protein supple-
mentation (13). Thus, protein supple-
mentation serves as an empirically
based means to maximize enhancements
in FFM during periods of resistance
training with anticipated improvements
ranging from 1 to 3 kg over approxi-
mately 12 weeks.
FORFEIT THE FAT, MAINTAIN THE
LEAN: OPTIMIZING WEIGHT LOSS
WITH PROTEIN
Weight loss through diet, exercise, or
a combination can confer a host of
benefits, including decreased cardio-
vascular disease risk, improved blood
lipid profile, and improved body com-
position. For individuals seeking to
lose weight, energy-restricted or hypo-
energetic diets are needed to induce
weight loss, but if restriction is severe,
the potential for skeletal muscle
atrophy and losses in LBM occur.
Research by Layman and Kerksick re-
veals that caloric prescriptions in
women that range from 1,200 to
1,600 calories per day in combination
with resistance-based exercise pro-
grams at a frequency of 3–5 d/wk for
90–150 minutes per week can promote
progressive weight loss without sharp
reductions in FFM (27,32). Restriction
of caloric intake below these levels
(500–1,000 kcal/d) is likely to induce
sharp reductions in body mass, with
a significant proportion of weight loss
coming from LBM. Weight loss of
this type can negatively impact met-
abolic rate and in athletic popula-
tions, recovery, and performance
(36,43), largely due to the reduction
seeninFFM.Inadditiontoprotein’s
ability to spare loss of FFM while re-
stricting calories, protein also helps in
dieting individuals due to its slower
overall digestibility when compared
with carbohydrate and fat and its
greater impact on satiety (40).
For these reasons, it is commonly
accepted that skeletal muscle plays a vital
role in maintaining metabolic rate and in
the performance of strength, power, and
endurance events, suggesting that a loss
of muscle may have negative metabolic
and performance outcomes. Moreover,
skeletal muscle loss and the associated
negative downregulation of one’s meta-
bolic rate are both commonly implicated
in the plateauing of weight loss and re-
gain after caloric restriction (26). In this
respect, elevated intakes of protein (1.5–
2.5 3the RDA: 1.2–2.0 g$kg
21
$d
21
),
particularly in the face of caloric restric-
tion and a basic resistance training
Strength and Conditioning Journal | www.nsca-scj.com 25
Table 1
Selected studies investigating the effect of protein supplementation on FFM
Author nProtein type (amount) Resistance-trained state RT program Training load DChange in
FFM (kg)
Burke et al.
2001 (10)
10 Whey (1.2
g$kg
21
$d
21
)
$3 y weight training
experience
4 d/wk,
6wk
4 sets/10–12
repetitions (8 d)
+2.3
4 sets/8–10
repetitions (8 d)
5 sets/6–8 repetitions
(8 d)
4 sets/8–10
repetitions (8 d)
4 sets/10–12
repetitions (8 d)
Cribb et al.
2006 (13)
6 Whey isolate (1.5
g$kg
21
$d
21
)
Recreational
bodybuilders, $2y
experience
3 d/wk 2 sets/8–10RM (70–
75% 1RM; wk 1–2)
+5 (62.8)
7 Casein (1.5
g$kg
21
$d
21
)
10 wk 2 sets/6RM (80–85%
1RM; wk 2–4)
+0.8 (62.4)
2–3 sets/4RM (90–
95% 1RM; wk 5–10)
Cribb et al.
2006 (12)
10 Whey isolate (1.5
g$kg
21
$d
21
)
Recreational
bodybuilders
10 wk 10RM (wk 1–2) +4.9 (62.5)
8–6RM (wk 3–6)
6–4RM (wk 7–10)
Fry et al.
2003 (20)
5 Whey (31.5 g) and
casein (43.5 g)
Recreationally trained 4 d/wk 4 sets/8–10
repetitions (70–
85% 1RM)
+1.6 (66.5)
Whey (7.5 g), casein
(7.5 g) and
colostrum (60 g)
12 wk +1.3 (65.9)
Hartman
et al.
2007 (19)
18 Fat-free fluid milk
(17.5 g)
Untrained 5 d/wk 2 sets/10–12
repetitions
(wk 1–2)
+3.9 (61.7)
12 wk 3 sets/10–12
repetitions
(wk 3–5)
4 sets/8–10
repetitions
(wk 6–7)
4 sets/6–8 repetitions
(wk 8–10)
+2.4 (62.5)
19 Fat-free soy protein
(17.5 g)
4 sets/4–6 repetitions
(wk 11–12)
Kerksick
et al. (34)
15 Whey (40 g), 5 g L-
glutamine, and 3 g
BCAAs
.1 y experience 4 d/wk 3 sets/10 repetitions
(wk 1–4)
20.1 (611.5)
VOLUME 37 | NUMBER 3 | JUNE 2015
26
program are commonly being used to
help attenuate FFM losses and promote
progressive weight loss. Whether the
individual is overweight and interested
in weight loss or an athlete interested
in enhancing their performance, the
question often surfaces: What amount
of each macronutrient, and more specif-
ically protein, should an individual
consume to achieve weight loss, yet
maintain skeletal muscle mass? Fortu-
nately, a good deal of published literature
is available discussing the optimal mac-
ronutrient profile that promotes fat loss
while synergistically maintaining (or
increasing) LBM, resulting in improved
body composition overall (31,38,55).
An early study by Walberg-Rankin
(61) found that males who resistance
trained and consumed low energy (18
kcal/kg) isocaloric diets containing
either moderate (0.8 g$kg
21
$d
21
)or
higher amounts of protein (1.6
g$kg
21
$d
21
) for just 7 days lost approx-
imately 3.8 kg. However, body protein
assessed through nitrogen balance
(NBAL) indicated that the moderate-
protein group exhibited a negative
NBAL of 23.19 g/d, whereas the
high-protein group had a positive
NBAL of 4.13 g/d (61). Briefly, a posi-
tive NBAL indicates that more protein
is being consumed than what is being
excreted by the body and is associated
with greater maintenance of LBM lev-
els. Later, Skov et al. (54) used a diet-
only approach to examine if a higher
protein diet would cause superior
weight loss in nonathletic, overweight,
and obese individuals. Participants con-
sumed a reduced calorie diet providing
low (12% of energy) or high (25% of
energy) amounts of protein. After 6
months, those consuming the higher
protein diet lost more weight (8.9 ver-
sus 5.1 kg) and more body fat (7.6 ver-
sus 4.3 kg) when compared with
individuals ingesting lower amounts
of dietary protein. Interestingly, 35%
of the subjects in the higher protein
group lost more than 10 kg, compared
Table 1
(continued)
10 wk 3 sets/8 repetitions
(wk 5–8)
3 sets/6 repetitions
(wk 9–10)
10 Whey (40 g) and casein
(8 g)
Abdominal crunch:
3 sets/25
repetitions wk
1–10
+1.8 (68.9)
Kerksick
et al. (33)
12 Whey (31.5 g) and
casein (43.5)
.1 y experience 4 d/wk 3 sets/10 repetitions
(wk 1–4)
+0.8 (613.5)
12 wk 3 sets/8 repetitions
(wk 5–8)
3 sets/6 repetitions
(wk 9–12)
13 Whey (7.5 g), casein
(7.5 g), and
colostrum (60 g)
Abdominal crunch:
3 sets/25
repetitions wk
1–12
+1.6 (13.6)
Lemon et al.
1992 (41)
12 Habitual diet + casein
and free amino
acids (2.62 g/kg)
Novice bodybuilders 6 d/wk 4 sets/#10
repetitions
(70–85% 1RM)
+0.1
4wk
Willoughby
et al.
2007 (53)
10 Whey and casein (14
g), free amino acids
(6 g)
Untrained 4 d/wk 3 sets/6–8 repetitions
(85–90% 1RM)
+5.62 (610.33)
10 wk
FFM 5fat-free mass; RM 5repetition maximum.
Strength and Conditioning Journal | www.nsca-scj.com 27
with only 9% of the lower protein
group (54). Since that time, research
examining high-protein diets on weight
loss and body composition improve-
ments (lowered fat mass and increased
or maintained FFM) in conjunction
with exercise have boomed. A summary
of these studies is provided in Table 2,
but numerous studies are available that
highlight the impact of restricted caloric
intake levels with higher amounts of
protein and in particular the power of
combining this dietary approach with
an exercise program. Research by
Layman et al. (37) reported that over-
weight adult women who ingested
a restricted calorie diet with a protein-
to-carbohydrate ratio of 1:4 (125 g of
protein day) lost a significantly greater
amount of weight as fat mass and dis-
played improvements in cholesterol, tri-
glycerides, and satiety, whereas another
similar study by the same research
group reported improvements in glu-
cose and insulin status in the individuals
who consumed higher amounts of pro-
tein (40). Finally, the combination of
a restricted calorie diet with higher
amounts of dietary protein in combina-
tion with exercise is the most powerful
weight loss stimulus (55), a concept
powerfully illustrated by a study pub-
lished where 4 groups of overweight
women followed a diet that was higher
in either dietary carbohydrate or dietary
protein with or without an additional
exercise program for a period of 4
months (38). As before, the women
who consumed a restricted calorie diet
higher in protein demonstrated greater
improvements in weight loss and fat
loss; the effect was further enhanced
when an exercise program was com-
bined with this dietary approach (38).
As illustrated throughout Table 2, evi-
dence exists for the favorable impact
of higher dietary protein intakes
toward the maintenance of LBM
during hypoenergetic weight loss in
overweight and obese populations
(19,28,31,37,38,42,46), especially with
a protein intake exceeding 30% total
calories (1,8). Caloric restriction and
weight loss in athletes is a popular issue
in weight-class sports (i.e., wrestling,
boxing, judo, etc.) or those activities that
have an aesthetic component to them
(i.e., gymnastics, dance, synchronized
swimming, diving, etc.), but must be ap-
proached with caution regardless of the
type of athlete. Toward this aim, severe
caloric restriction in an athlete who is
involved in high volumes of training,
practice, and competition can negatively
impact performance, promote loss of
FFM, hinder recovery, increase suscep-
tibility to illness, and set the stage for
overtraining. In addition, coaches and
athletes should also be aware of the psy-
chological burden associated with calo-
ric restriction. Fundamentally, the
processofweightlossisnodifferent
than any other population, but with
pressure from coaches to lose weight
as quickly as possible, the recipe for con-
cern becomes evident. For this reason,
athletes are encouraged to work hard to
lose weight and modify their body com-
positiontomeetsuchgoalsduringthe
off-season and even then, the rate of
weight loss must be adjusted to allow
for increases in skill development and
physical performance. A few studies
do exist that have targeted diet ap-
proaches in active and athletic popula-
tions. For example, Pasiakos et al. (47)
compared diets providing protein at 0.8,
1.6, and 2.4 g$kg
21
$d
21
,13,23,and
33the RDA for protein, respectively,
while achieving a 40% energy deficit
through diet and exercise in physically
active military personnel for a 3-week
period. Participants lost an average of
3.2 kg regardless of group, but the pro-
portion of weight loss due to specific
changes in FFM and fat mass was most
favorable in those individuals whose
dietary protein intake was 1.6 and
2.4 g$kg
21
$d
21
. Furthermore, Mettler
et al. (43) examined the influence of die-
tary protein status on changes in body
composition and performance during
a short-term hypoenergetic diet in com-
peting athletes. The athletes were fed
a hypoenergetic diet (60% of habitual
energy intake), containing either 15%
(;1.0 g$kg
21
$d
21
) protein or 35%
(;2.3 g$kg
21
$d
21
) protein for 2 weeks.
The results indicated that greater pro-
tein consumption led to a significantly
superior maintenance of LBM when
compared with the lower protein intake,
whereas performance outcomes (1RM
bench press, squat jump, maximal iso-
metric leg extension, endurance bench
press, and Wingate) were not altered,
regardless of diet (43). Finally, an excel-
lent study by Garthe et al. over 1 year
examined the impact of 2 different rates
of weight loss (both were slower than
what is typically achieved for nonath-
letes) and found that after 6 months of
dieting, a slower rate of weight loss facil-
itated greater levels of lean mass and
strength,butafter12months,the
amount of weight lost, body composi-
tion, and performance changes were
similar (22). An excellent review on
weight loss considerations in athletes
was published by Turocy et al. as a posi-
tion stand for the National Athletic
Trainers Association (60).
To extend the practicality of our arti-
cle, a brief discussion will be included
highlighting absolute amounts of calo-
ries and protein consumed during pub-
lished weight loss studies. For example,
Layman’s classic block design involved
diets with higher carbohydrate and
higher protein amounts with and with-
out the addition of exercise and
required the women (45–47 years;
79.8–91.1 kg; 30.2–35.4 kg/m
2
) in their
research to ingest approximately 1,700
calories per day. The higher carbohy-
drate diet delivered protein at 0.8
g$kg
21
$d
21
(15% total caloric intake)
and lipids at 30% of total caloric intake.
The carbohydrate:protein ratio in this
diet group was .3.5. However, the
protein group delivered protein at 1.6
g$kg
21
$d
21
(;30% total calories) and
fat remained at 30% total calories. The
carbohydrate:protein ratio for this diet
group was subsequently ,1.5. Both
diets delivered the same absolute amount
of calories (;1,700 calories), total fat
(;57 g/d), and fiber (;17 g/ d ). Th i s
dietary approach was combined with
a modest exercise program consisting
of 150 min/wk (30 minutes for 5 d/wk)
of walking and a whole-body resis-
tance training program 2 d/wk
(7 machine-based exercises for all
major muscle groups, one 12RM
set was performed on each exercise).
VOLUME 37 | NUMBER 3 | JUNE 2015
28
Table 2
Selected studies investigating high-protein versus low-protein diets on weight loss in various populations
Author Population of subjects Duration Diet intervention Weight loss (kg) Conclusions
Walberg,
1988 (52)
Recreational weight
lifters
7 d Hypoenergetic diets
(18 kcal/d)
3.8 Hypoenergetic diet providing
twice the RDA for protein (1.6
g$kg
21
$d
21
) was more
effective in retaining body
protein in WL than a diet with
higher carbohydrate but the
RDA for protein
Group 1: 0.8 g
PRO/kg/d
Group 2: 1.6 g
PRO/kg/d
Skov,
1999 (45)
Overweight and obese
men and women
6 mo Ad libitum fat-
reduced diets
(30% of total
energy)
Group 1: 5.1 Replacement of some dietary
carbohydrate by protein in an
ad libitum fat-reduced diet
improves weight loss and
increases the proportion of
subjects achieving a clinically
relevant weight loss
Group 1: high
carbohydrate,
12% protein
Group 2: 8.9
Group 2: high
protein, 25%
protein
Kerksick,
2009 (27)
Sedentary, obese
women
14 wk CON: no exercise,
no diet
VLCHP: 5.2 Greatest improvements
occurred when carbohydrate
was replaced with protein in
the diet. All groups improved
muscular fitness, no
difference between groups
ND: no diet, exercise LCMP: 4.0
HEHCLP: 2,600 kcal,
55:15:30%
HCLP: 3.8
VLCHP: 1,200 kcal,
63:7:30%
LCMP: 1,200 kcal,
50:20:30%
HCLP: 1,200 kcal,
55:15:30%
(continued)
Strength and Conditioning Journal | www.nsca-scj.com 29
A close investigation of the Figure
revealed significant changes in body
fatness for both higher protein
groupsandwhenexercisewas
added, even greater amounts of fat
were lost. Kerksick et al. used diets
that ranged in caloric intakes (1,200–
1,600 kcals/d) and protein intake (15–
63% protein) over a 14-week period in
obese women and found greater weight
and fat loss when higher protein intakes
were consumed. Although the majority
Table 2
(continued)
Mettler,
2010 (36)
Resistance-trained
athletes
2 wk Hypoenergetic (40%
energy reduction)
Group 1: 3.0 35% protein was significantly
superior to 15% energy
protein for maintenance of
LBM during short-term
hypoenergetic weight loss
Group 1: ;1.0
g$kg
21
$d
21
, 15%
PRO
Group 2: 1.5
Group 2: ;2.3
g$kg
21
$d
21
, 35%
PRO
Josse, 2011
(24)
Healthy, overweight,
and obese women
16 wk HPHD (30% PRO and
15% dairy)
4.3 HPHD group: greater total fat
and visceral fat losses, greater
lean mass gains, and increases
in strength despite similar
body weight loss between all
groups
APMD (15% PRO and
7.5% dairy)
APLD (15% PRO and
,2% dairy)
Wycherley,
2012 (64)
General population Meta-
analysis
12.1 6
9.3 wk
Hypoenergetic diets,
which were
isocaloric
Group 1: 20.8 Compared with the standard
protein, high-protein diets
caused a 0.87 kg decrease
in FM and mitigation of
reductions in FFM, 0.43 kg
Group 1: high
protein, low fat
Group 2: standard
protein, low fat
Pasiakos, 2013
(47)
Physically active
military personnel
3 wk Hypoenergetic (40%
energy reduction)
3.2 Proportion of WL due to reduced
FFM was lower and the loss of
FM was higher in those receiving
1.6 and 2.3 g$kg
21
$d
21
Group 1: 0.8
g$kg
21
$d
21
Group 2: 1.6
g$kg
21
$d
21
Group 3: 2.3
g$kg
21
$d
21
APLD 5adequate protein, low dairy; APMD 5adequate protein, medium dairy; CON 5control; FFM 5fat-free mass; FM 5fat mass; HCLP 5
high-carbohydrate, low-protein diet; HEHCLP 5high-energy, high-carbohydrate, low-protein diet; HPHD 5high protein, high dairy; LBM 5lean
body mass; LCMP 5low-carbohydrate, moderate-protein diet; ND 5no diet; PRO 5protein; RDA 5recommended daily allowance; VLCHP 5very
low carbohydrate, high-protein diet; WL 5weight loss.
VOLUME 37 | NUMBER 3 | JUNE 2015
30
of weight loss literature has used women
as study participants, prescribed hypoe-
nergetic levels in men are commonly
between 1,800 and 2,200 calories (55)
with similar amounts and distribution
of the macronutrients. Thus, people
interested in applying these findings in
women might start with a caloric pre-
scription of approximately 1,500–1,700
cal/d with protein contents around
30–40% of total caloric intake, whereas
in men, suggested values may be 1,800–
2,000 calories with similar protein con-
tents. These approximations are only
starting points, and from there, the
practitioner must monitor compli-
ance, energy, and body composition
changes and adjust initial caloric and
protein levels accordingly.
In summary, when consuming
a reduced-energy diet, the content of
protein as well as overall energy intake
strongly impacts the degree to which
fat and FFM are lost from the body. In
general, athletic or nonathletic individ-
uals, regardless of body mass index sta-
tus, who are aiming to decrease their
body weight, may be advised to keep
protein intake high ($1.5 g$kg
21
$d
21
).
This diet strategy will allow individuals
to mitigate losses of LBM, which over
extended periods of restricted energy
will sustain metabolic rate levels and
promote greater losses of fat mass
while maintaining performance.
CONCLUSIONS
Protein is an important nutrient that
should be consumed in higher
amounts by most individuals, particu-
larly exercising individuals. Additional
considerations of protein as they relate
to timing and meal patterns continue
to garner a great deal of attention.
Although more research is needed,
current findings indicate that protein
consumption surrounding a workout
has the potential to impact adaptations
to exercise training, particularly when
total protein intake does not meet
bodily demands. Other work suggests
that consuming a regular distribution
of protein across the day may promote
favorable changes in MPS and markers
of health. As an approach to lose
weight, diets that are restricted in cal-
ories and higher in protein consistently
indicate favorable, and in many cases,
greater improvements in weight loss
and fat loss as well as maintenance of
LBM. Similarly, elevated protein and
amino acid intake in conjunction with
resistance exercise is the most effective
stimulus to instigate favorable im-
provements in FFM and strength.
In conclusion, the following take-
home points are provided:
From a timing of nutrients perspec-
tive, research involving both protein
and carbohydrate indicate that
total absolute intake is an important
consideration. In both instances,
any beneficial impact of protein
timing seems to be diminished
(or eliminated altogether) when
absolute intake of protein (1.2–
1.6 g$kg
21
$d
21
) achieves levels com-
mensurate with activity levels.
In a similar fashion, coingestion of
carbohydrate with protein has
potential to favorably impact rates
of muscle glycogen recovery, but this
effect is most predominant when
absolute daily intake of carbohy-
drates are not of a level that is
commensurate with activity levels
(7–10 g$kg
21
$d
21
).
Available research does indicate that
postexercise ingestion of protein may
exert favorable outcomes, such as im-
provements in strength and FFM.
When this research is performed
in untrained or individuals with
only minimal exposure to exercise
training, the impact of timing is likely
greater, an outcome that is more likely
to do with the training status and
known changes in protein metabolism.
Consuming multiple ($3) doses of
protein in intermediate sizes doses
(20–25 g) throughout the day may
favorably impact changes in MPS
and overall changes in body mass,
fat mass, and FFM.
In combination with a heavy resis-
tance training program (4–5 d/wk,
multijoint exercises, 3–4 sets of
6–10RM loads [70–85% 1RM], and
2-minute rest between sets), elevated
intakes of dietary protein (1.2–
1.6 g$kg
21
$d
21
) have been clearly
shownintheliteraturetopromote
greater accretion of strength and FFM.
Modest caloric restriction (women:
1,400–1,600 calories and men:
1,800–2,000 calories) in combination
with a consistent exercise program
Figure. Changes in relative body fatness (%fat) for adult women after 16 weeks of
consuming reduced-energy diets with a ratio of carbohydrates:protein
.3.5 (CHO) or ,1.5 (PRO) with or without a supervised exercise program
(EX: 5 d/wk walking and 2 d/wk resistance training). Values are mean 6
SEM, n512. *Significant main effect of diet, p,0.05. #Significant main
effect of exercise, p,0.05. Used with permission. Original source: Layman
DK, et al. J Nutr 1903–1910, 2005.
Strength and Conditioning Journal | www.nsca-scj.com 31
that combines aerobic and resistance
exercise (4–5 d/wk, 170–200 min/wk)
is an effective long-term approach to
losing body mass with a majority of
this coming from fat mass.
Modest replacement of carbohydrate
with protein (carbohydrate: protein
ratio of .3.5, or protein content of
30–40% of total calories) has been
shown to further promote fat loss,
minimize loss of FFM, and also pro-
mote improvements in glucose, insu-
lin, triglyceride, and cholesterol levels.
Conflicts of Interest and Source of Funding:
The authors report no conflicts of interest
and no source of funding.
Kurt A.
Escobar is
adoctoral
student and
teaching assis-
tant in the
Department of
Health, Exer-
cise, and Sports
Sciences at the University of
New Mexico.
Trisha A.
McLain is cur-
rently a PhD
student in the
Health, Exercise,
and Sports Sci-
ence Department
at the University
of New Mexico.
Chad M.
Kerksick is cur-
rently an Assistant
Professor of Exer-
cise Science in the
Exercise Science
department in the
School of Sport, Recreation and Exercise
Sciences at Lindenwood University.
REFERENCES
1. Alford BB, Blankenship AC, and
Hagen RD. The effects of variations in
carbohydrate, protein, and fat content of
the diet upon weight loss, blood values, and
nutrient intake of adult obese women. JAm
Diet Assoc 90: 534–540, 1990.
2. Andersen LL, Tufekovic G, Zebis MK,
Crameri RM, Verlaan G, Kjaer M, Suetta C,
Magnusson P, and Aagaard P. The effect of
resistance training combined with timed
ingestion of protein on muscle fiber size
and muscle strength. Metabolism 54: 151–
156, 2005.
3. Antonio J, Peacock CA, Ellerbroek A,
Fromhoff B, and Silver T. The effects of
consuming a high protein diet (4.4 g/kg/d) on
body composition in resistance-trained
individuals. J Int Soc Sports Nutr 11: 19, 2014.
4. Aragon AA and Schoenfeld BJ. Nutrient
timing revisited: Is there a post-exercise
anabolic window? J Int Soc Sports Nutr
10: 5, 2013.
5. Arciero PJ, Baur D, Connelly S, and
Ormsbee MJ. Timed-daily ingestion of whey
protein and exercise training reduces
visceral adipose tissue mass and improves
insulin resistance: The PRISE study. J Appl
Physiol (1985) 117: 1–10, 2014.
6. Areta JL, Burke LM, Ross ML, Camera DM,
West DW, Broad EM, Jeacocke NA,
Moore DR, Stellingwerff T, Phillips SM,
Hawley J, and Coffey VG. Timing and
distribution of protein ingestion during
prolonged recovery from resistance exercise
alters myofibrillar protein synthesis. JPhysiol
591: 2319–2331, 2013.
7. Austin K and Seebohar B. Performance
Nutrition: Applying the Science of Nutrient
Timing. Champaign, IL: Human Kinetics,
2011.
8. Ballor DL and Poehlman ET. Exercise-
training enhances fat-free mass
preservation during diet-induced weight
loss: A meta-analytical finding. Int J Obes
Relat Metab Disord 18: 35–40, 1994.
9. Bolster DR, Pikosky MA, Gaine PC,
Martin W, Wolfe RR, Tipton KD, Maclean D,
Maresh CM, and Rodriguez NR. Dietary
protein intake impacts human skeletal
muscle protein fractional synthetic ratesafter
endurance exercise. Am J Physiol
Endocrinol Metab 289: E678–E683, 2005.
10. Borsheim E, Aarsland A, and Wolfe RR.
Effect of an amino acid, protein, and
carbohydrate mixture on net muscle protein
balance after resistance exercise. Int J Sport
Nutr Exerc Metab 14: 255–271, 2004.
11. Borsheim E, Tipton KD, Wolf SE, and
Wolfe RR. Essential amino acids and
muscle protein recovery from resistance
exercise. Am J Physiol Endocrinol Metab
283: E648–E657, 2002.
12. Burke DG, Chilibeck PD, Davidson KS,
Candow DG, Farthing J, and Smith-Palmer T.
The effect of whey protein supplementation
with and without creatine monohydrate
combined with resistance training on lean
tissue mass and muscle strength. Int J Sport
Nutr Exerc Metab 11: 349 –364, 2 001.
13. Cermak NM, Res PT, de Groot LC,
Saris WH, and van Loon LJ. Protein
supplementation augments the adaptive
response of skeletal muscle to resistance-
type exercise training: A meta-analysis. Am
J Clin Nutr 96: 1454–1464, 2012.
14. Churchward-Venne TA, Murphy CH,
Longland TM, and Phillips SM. Role of
protein and amino acids in promoting lean
mass accretion with resistance exercise
and attenuating lean mass loss during
energy deficit in humans. Amino Acids 45:
231–240, 2013.
15. Coyle EF, Coggan AR, Hemmert MK,
Lowe RC, and Walters TJ. Substrate usage
during prolonged exercise following
a preexercise meal. J Appl Physiol (1985)
59: 429–433, 1985.
16. Cribb PJ and Hayes A. Effects of
supplement timing and resistance exercise
on skeletal muscle hypertrophy. Med Sci
Sports Exerc 38: 1918–1925, 2006.
17. Cribb PJ, Williams AD, Carey MF, and
Hayes A. The effect of whey isolate and
resistance training on strength, body
composition, and plasma glutamine. Int J
Sport Nutr Exerc Metab 16: 494–509,
2006.
18. Cribb PJ, Williams AD, and Hayes A. A
creatine-protein-carbohydrate supplement
enhances responses to resistance training.
Med Sci Sports Exerc 39: 1960–1968, 2007.
19. Frestedt JL, Zenk JL, Kuskowski MA, W ard LS,
and Bastian ED. A whey-protein supplement
increases fat loss and spares lean muscle in
obese subjects: A randomized human clinical
study. Nutr Metab (Lond) 5: 8, 2008.
20. Fry AC, Schilling BK, Chui L, Weiss LW,
Kreider R, and Rasmussen CJ. Muscle fiber
and performance adaptations to resistance
exercise with Myovive, colostrum or casein
and whey supplementation. Res Sports
Med 11: 109–127, 2003.
21. Fujita S, Dreyer HC, Drummond MJ,
Glynn EL, Volpi E, and Rasmussen BB.
Essential amino acid and carbohydrate
ingestion before resistance exercise does
not enhance postexercise muscle protein
synthesis. J Appl Physiol (1985) 106:
1730–1739, 2009.
VOLUME 37 | NUMBER 3 | JUNE 2015
32
22. Garthe I, Raastad T, and Sundgot-
Borgen J. Long-term effect of weight loss
on body composition and performance in
elite athletes. Int J Sport Nutr Exerc Metab
21: 426–435, 2011.
23. Hartman JW, Tang JE, Wilkinson SB,
Tarnopolsky MA, Lawrence RL, Fullerton AV,
and Phillips SM. Consumption of fat-free
fluid milk after resistance exercise promotes
greater lean mass accretion than does
consumption of soy or carbohydrate in
young, novice, male weightlifters. Am J Clin
Nutr 86: 373–381, 200 7.
24. Hoffman JR, Ratamess NA, Tranchina CP,
Rashti SL, Kang J, and Faigenbaum AD.
Effect of protein-supplement timing on
strength, power, and body-composition
changes in resistance-trained men. Int J
Sport Nutr Exerc Metab 19: 172–185, 2009.
25. Hulmi JJ, Lockwood CM, and Stout JR.
Effect of protein/essential amino acids and
resistance training on skeletal muscle
hypertrophy: A case for whey protein. Nutr
Metab (Lond) 7: 51, 2010.
26. Hunter GR, Brock DW, Byrne NM,
Chandle r-Laney PC, Del Corral P, and
Gower BA. Exercise training prevents regain
of visceral fat for 1 year following weightloss.
Obesity (Silver Spring) 18: 690 –695, 2010.
27. Ivy JL, Goforth HW Jr, Damon BM,
McCauley TR, Parsons EC, and Price TB.
Early postexercise muscle glycogen
recovery is enhanced with a carbohydrate-
protein supplement. J Appl Physiol (1985)
93: 1337–1344, 2002.
28. Josse AR, Atkinson SA, Tarnopolsky MA,
and Phillips SM. Increased consumption of
dairy foods and protein during diet- and
exercise-induced weight loss promotes fat
mass loss and lean mass gain in
overweight and obese premenopausal
women. J Nutr 141: 1626–1634, 2011.
29. Kerksick C, ed. Nutrient Timing: Metabolic
Optimization for Health, Performance and
Recovery. Boca Raton, FL: CRC Press,
2010.
30. Kerksick C, Harvey T, Stout J, Campbell B,
Wilborn C, Kreider R, Kalman D,
Ziegenfuss T, Lopez H, Landis J, Ivy JL, and
Antonio J. International Society of Sports
Nutrition position stand: Nutrient timing.
J Int Soc Sports Nutr 5: 17, 2008.
31. Kerksick C, Thomas A, Campbell B,
Taylor L, Wilborn C, Marcello B, Roberts M,
Pfau E, Grimstvedt M, Opusunju J,
Magrans-Courtney T, Rasmussen C,
Wilson R, and Kreider RB. Effects of
a popular exercise and weight loss
program on weight loss, body composition,
energy expenditure and health in obese
women. Nutr Metab (Lond) 6: 23, 2009.
32. Kerksick CM and Kulovitz MG.
Requirements of protein, carbohydrates
and fats for athletes. In: Nutrition and
Enhanced Sports Performance:
Recommendations for Muscle Building.
Bagchi D, Nair S, and Sen CK, eds.
Waltham, MA: Elsevier Publishers, 2013.
33. Kerksick CM, Rasmussen C, Lancaster S,
Starks M, Smith P, Melton C,
Greenwood M, Almada A, and Kreider R.
Impact of differing protein sources and
a creatine containing nutritional formula
after 12 weeks of resistance training.
Nutrition 23: 647–656, 2007.
34. Kerksick CM, Rasmussen CJ,
Lancaster SL, Magu B, Smith P, Melton C,
Greenwood M, Almada AL, Earnest CP,
and Kreider RB. The effects of protein and
amino acid supplementation on
performance and training adaptations
during ten weeks of resistance training.
J Strength Cond Res 20: 643–653, 2006.
35. Koopman R, Saris WH, Wagenmakers AJ,
and van Loon LJ. Nutritional interventions to
promote post-exercise muscle protein
synthesis. Sports Med 37: 895–906, 2007.
36. Layman DK. Protein quantity and quality at
levels above the RDA improves adult weight
loss. JAmCollNutr23: 631S–636S, 2004.
37. Layman DK, Boileau RA, Erickson DJ,
Painter JE, Shiue H, Sather C, and
Christou DD. A reduced ratio of dietary
carbohydrate to protein improves body
composition and blood lipid profiles during
weight loss in adult women. J Nutr 133:
411–417, 2003.
38. Layman DK, Evans E, Baum JI, Seyler J,
Erickson DJ, and BoileauRA. Dietary protein
and exercise have additive effects on body
composition during weight loss in adult
women. JNutr135: 1903–1910, 2005.
39. Layman DK, Shiue H, Sather C,
Erickson DJ, and Baum J. Increased dietary
protein modifies glucose and insulin
homeostasis in adult women during weight
loss. J Nutr 133: 405–410, 2003.
40. Leidy HJ, Armstrong CL, Tang M,
Mattes RD, and Campbell WW. The
influence ofhigher protein intake and greater
eating frequency on appetite control in
overweight and obese men. Obesity (Silver
Spring) 18: 1725–1732, 2010.
41. Lemon PW, Tarnopolsky MA, MacDougall JD,
and Atkinson SA. Protein requirements and
muscle mass/strength changes during
intensive training in novice bodybuilders.
J Appl Physiol 73(2): 767–775, 1992.
42. Meckling KA and Sherfey R. A randomized
trial of a hypocaloric high-protein diet, with
and without exercise, on weight loss, fitness,
and markers of the metabolic syndrome in
overweight and obese women. Appl Physiol
Nutr Metab 32: 743–752, 200 7.
43. Mettler S, Mitchell N, and Tipton KD.
Increased protein intake reduces lean body
mass loss during weight loss in athletes.
Med Sci Sports Exerc 42: 326–337, 2010.
44. Miller SL, Maresh CM, Armstrong LE,
Ebbeling CB, Lennon S, and Rodriguez NR.
Metabolic response to provision of mixed
protein-carbohydrate supplementation
during endurance exercise. Int J Sport Nutr
Exerc Metab 12: 384–397, 2002.
45. Moore DR, Areta J, Coffey VG, Stellingwerff T,
Phillips SM, Burke LM, Cleroux M, Godin JP,
and Hawley JA. Daytime pattern of post-
exercise protein intake affects whole-body
protein turnover in resistance-trained males.
Nutr Metab (Lond) 9: 91, 2012.
46. Noakes M, Keogh JB, Foster PR, and
Clifton PM. Effect of an energy-restricted,
high-protein, low-fat diet relative to
a conventional high-carbohydrate, low-fat
diet on weight loss, body composition,
nutritional status, and markers of
cardiovascular health in obese women. Am
J Clin Nutr 81: 1298–1306, 2005.
47. Pasiakos SM, Cao JJ, Margolis LM, Sauter ER,
Whigham LD, McClung JP, Rood JC,
Carbone JW, Combs GF Jr, and Young AJ.
Effects of high-protein diets on fat-free mass
and muscle protein synthesis following weight
loss: A randomized controlled trial. FASEB J
27: 3837–3847, 2013.
48. Phillips SM. Protein requirements and
supplementation in strength sports.
Nutrition 20: 689–695, 2004.
49. Phillips SM, Tang JE, and Moore DR. The role
of milk- and soy-based protein in support of
muscle protein synthesis and muscle protein
accretion in young and elderly persons. JAm
Coll Nutr 28: 343–354, 2009.
50. Saunders MJ, Kane MD, and Todd MK.
Effects of a carbohydrate-protein beverage on
cycling endurance and muscle damage. Med
Sci Sports Exerc 36: 1233–1238, 2004.
51. Saunders MJ, Moore RW, Kies AK,
Luden ND, and Pratt CA. Carbohydrate and
protein hydrolysate coingestions improvement
of late-exercise time-trial performance. Int J
Sport Nutr Exerc Metab 19: 136–149, 2009.
52. Schoenfeld BJ, Aragon AA, and Krieger JW.
The effect of protein timing on muscle
strength and hypertrophy: A meta-analysis.
JIntSocSportsNutr10: 53, 2013.
53. Skolnik H and Chernus A. Nutrient Timing
for Peak Performance. Champaign, IL:
Human Kinetics, 2010.
54. Skov AR, Toubro S, Ronn B, Holm L, and
Astrup A. Randomized trial on protein vs
Strength and Conditioning Journal | www.nsca-scj.com 33
carbohydrate in ad libitum fat reduced diet
for the treatment of obesity. Int J Obes
Relat Metab Disord 23: 528–536, 1999.
55. Stiegler P and Cunliffe A. The roleof diet and
exercise for the maintenance of fat-free mass
and resting metabolic rate during weight
loss. Sports Med 36: 239–262, 2006.
56. Tipton KD, Elliott TA, Cree MG,
Aarsland AA, Sanford AP, and Wolfe RR.
Stimulation of net muscle protein synthesis
by whey protein ingestion before and after
exercise. Am J Physiol Endocrinol Metab
292: E71–E76, 2007.
57. Tipton KD, Ferrando AA, Phillips SM,
Doyle D Jr, and Wolfe RR. Postexercise net
protein synthesis in human muscle from
orally administered amino acids. Am J
Physiol 276: E628–E634, 1999.
58. Tipton KD, Rasmussen BB, Miller SL,
Wolf SE, Owens-Stovall SK, Petrini BE, and
Wolfe RR. Timing of amino acid-carbohydrate
ingestion alters anabolic response of muscle
to resistance exercise. Am J Physiol
Endocrinol Metab 281: E197–E206, 2001.
59. Tipton KD and Wolfe RR. Exercise, protein
metabolism, and muscle growth. Int J Sport
Nutr Exerc Metab 11: 109–132, 2001.
60. Turocy PS, DePalma BF, Horswill CA,
Laquale KM, Martin TJ, Perry AC, Somova MJ,
and Utter AC. National athletic trainers’
associationpositionstatement:Safeweight
loss and maintenance practices in sport and
exercise. JAthlTrain46: 322–336, 2011.
61. Walberg-Rankin J. Changing Body Weight
and Composition in Athletes. Carmel, IN:
Cooper Publishing Group, 1988.
62. Widrick JJ, Costill DL, Fink WJ, Hickey MS,
McConell GK, and Tanaka H.
Carbohydrate feedings and exercise
performance: Effect of initial muscle
glycogen concentration. J Appl Physiol
(1985) 74: 2998–3005, 1993.
63. Willoughby DS, Stout JR, and
Wilborn CD. Effects of resistance
training and protein plus amino acid
supplementation on muscle anabolism,
mass, and strength. Amino Acids 32:
467–477, 2007.
64. Wycherley TP, Moran LJ, Clifton PM,
Noakes M, and Brinkworth GD. Effects of
energy-restricted high-protein, low-fat
compared with standard-protein, low-fat
diets: a meta-analysis of randomized
controlled trials. Am J Clin Nutr 96: 1281–
1298, 2012.
65. Zawadzki KM, Yaspelkis BB III, and Ivy JL.
Carbohydrate-protein complex increases
the rate of muscle glycogen storage after
exercise. J Appl Physiol (1985) 72: 1854–
1859, 1992.
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