ArticlePDF Available

Coingestion of Carbohydrate and Protein on Muscle Glycogen Synthesis after Exercise: A Meta-analysis

Authors:

Abstract and Figures

Evidence suggests that carbohydrate and protein (CHO-PRO) ingestion after exercise enhances muscle glycogen repletion to a greater extent than carbohydrate (CHO) alone. However, there is no consensus at this point, and results across studies are mixed, which may be attributable to differences in energy content and carbohydrate intake relative to body mass consumed after exercise. The purpose of this study was determine the overall effects of CHO-PRO and the independent effects of energy and relative carbohydrate content of CHO-PRO supplementation on post-exercise muscle glycogen synthesis compared to CHO alone. Methods: Meta-analysis was conducted on crossover studies assessing the influence of CHO-PRO compared to CHO alone on post-exercise muscle glyocgen synthesis. Studies were identified in a systematic review from Pubmed and Cochrane Library databases. Data are presented as effect size [ES(95%CI)] using Hedges' g. Subgroup analyses were conducted to evaluate effects of isocaloric and non-isocaloric energy content, and dichotomized by median relative carbohydrate (high: ≥0.8g/kg/hr, low: <0.8g/kg/hr) content on glycogen synthesis. Results: 20 studies were included in the analysis. CHO-PRO had no overall effect on glycogen synthesis [0.13(-0.04,0.29)] compared to CHO. Subgroup analysis found that CHO-PRO had a positive effect [0.26(0.04,0.49)] on glycogen synthesis when the combined intervention provided more energy than CHO. Glycogen synthesis was not significant [-0.05(-0.23,0.13)] in CHO-PRO compared to CON when matched for energy content. There was no statistical difference of CHO-PRO on glycogen synthesis in high [0.07(-0.11,0.25)] or low [0.21(-0.08,0.50)] carbohydrate content compared to CHO. Conclusion: Glycogen synthesis rates are enhanced when CHO-PRO are coingested after exercise compared to CHO only when the added energy of protein is consumed in addition to, not in place of, carbohydrate.
Content may be subject to copyright.
Downloaded from https://journals.lww.com/pages by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdtwnfKZBYtws= on 01/09/2021
Downloadedfromhttps://journals.lww.com/pages by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdtwnfKZBYtws= on 01/09/2021
Coingestion of Carbohydrate and Protein on
Muscle Glycogen Synthesis after Exercise:
A Meta-analysis
LEE M. MARGOLIS
1
, JILLIAN T. ALLEN
1,2
, ADRIENNE HATCH-MCCHESNEY
1
, and STEFAN M. PASIAKOS
1
1
Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine, Natick, MA; and
2
Oak Ridge Institute of
Science and Education, Oak Ridge, TN
ABSTRACT
MARGOLIS, L. M., J. T. ALLEN, A. HATCH-MCCHESNEY, and S. M. PASIAKOS. Coingestion of Carbohydrate and Protein on Muscle
GlycogenSynthesis after Exercise: A Meta-analysis. Med. Sci. Sports Exerc., Vol. 53, No. 2, pp. 384393, 2021. Introduction/Purpose: Ev-
idence suggests thatcarbohydrate andprotein (CHO-PRO) ingestionafter exercise enhances muscle glycogenrepletion to a greaterextent than
carbohydrate (CHO) alone. However, there is no consensus at this point, and results across studies are mixed, which may be attributable to
differences in energy content and carbohydrate intake relativeto body mass consumed after exercise. The purpose of this study was determine
the overall effects of CHO-PRO and the independent effects of energy and relative carbohydrate content of CHO-PRO supplementation on
postexercise muscle glycogen synthesis compared with CHO alone. Methods: Meta-analysis was conducted on crossover studies assessing
the influence of CHO-PRO compared with CHO alone on postexercise muscle glycogen synthesis. Studies were identified in a systematic
review from PubMed and Cochrane Library databases. Data are presented as effect size (95% confidence interval [CI]) using Hedgesg. Sub-
group analyses were conducted to evaluate effects of isocaloric and nonisocaloric energy content and dichotomized by median relative carbo-
hydrate (high, 0.8 g·kg
1
h
1
; low, <0.8 g·kg
1
h
1
) content on glycogen synthesis. Results: Twenty studies were included in the analysis.
CHO-PRO had no overall effect on glycogen synthesis (0.13, 95% CI = 0.04 to 0.29) compared with CHO. Subgroup analysis found that
CHO-PRO had a positive effect (0.26, 95% CI = 0.040.49) on glycogen synthesis when the combined intervention provided more energy
than CHO. Glycogen synthesis was not significant (0.05, 95% CI = 0.23 to 0.13) in CHO-PRO compared with CON when matched for
energy content. There was no statistical difference of CHO-PRO on glycogen synthesis in high (0.07, 95% CI = 0.11 to 0.22) or low
(0.21, 95% CI = 0.08 to 0.50) carbohydrate content compared with CHO. Conclusion: Glycogen synthesis rates are enhanced when
CHO-PRO are coingested after exercise compared with CHO only when the added energy of protein is consumed in addition to, not in place
of, carbohydrate. Key Words: ENDURANCE EXERCISE, AEROBIC EXERCISE, EXERCISE RECOVERY, SUPPLEMENT
It is well known that modulating postexercise nutrition is
an effective approach to facilitate replenishment of muscle
glycogen stores in athletes or military service members
who train, compete, and perform sustained physically demand-
ing tasks multiple times per day (1). To maximally stimulate
glycogen synthesis, current sport nutrition recommendations
are to consume 1.2 g of carbohydrate per kilogram body mass
per hour for 46 h postexercise (1). Consumption of0.3 g·kg
1
body mass of a high-quality protein is also recommended to
aidinpostexerciserecoverybystimulatingmuscleprotein
synthesis and repair (1). Some evidence suggests that coingestion
of carbohydrate and protein (CHO-PRO) after exercise may stim-
ulate greater glycogen synthesis during recovery compared with
carbohydrate (CHO) alone (2,3). This greater glycogen synthesis
has been attributed to the insulinotropic effects of amino acids, such
as leucine, on pancreatic release of insulin (4,5), resulting in higher
circulating insulin concentrations thereby increasing muscle glucose
uptake when CHO-PRO is consumed compared with CHO alone
(6,7). Furthermore, consuming CHO-PRO after exercise may en-
hance glycogen synthesis to a greater extent than CHO alone by
upregulating markers of glycogen synthase activity (8).
Despite evidence of greater glucose uptake and molecular
regulation of glycogen synthesis, the observed effect of
CHO-PRO ingestion on postexercise glycogen synthesis as
Address for correspondence: Lee M. Margolis, Ph.D., Military Nutrition Division,
U.S. Army Research Institute of Environmental Medicine, 10 General Greene
Avenue, Bldg. 42, Natick, MA 01760; E-mail: lee.m.margolis.civ@mail.mil.
Submitted for publication May 2020.
Accepted for publication July 2020.
Supplemental digital content is available for this article. Direct URL citations
appear in the printed text and are provided in the HTML and PDF versions
of this article on the journals Web site (www.acsm-msse.org).
0195-9131/20/5302-0384/0
MEDICINE & SCIENCE IN SPORTS & EXERCISE
®
Copyright © 2020 The Author(s). Published by Wolters Kluwer Health, Inc.
on behalf of the American College of Sports Medicine. This is an open-access
article distributed under the terms of the Creative Commons Attribution-Non
Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permis-
sible to download and share the work provided it is properly cited. The work
cannot be changed in any way or used commercially without permission from
the journal.
DOI: 10.1249/MSS.0000000000002476
384
APPLIED SCIENCES
compared with CHO alone is inconsistent. Both positive
(911) and null (1214) effects of CHO-PRO ingestion com-
pared with CHO have been reported. The discordant results
across studies may arise because some used isocaloric
CHO-PRO and CHO interventions, whereas others used
nonisocaloric interventions. van Loon et al. (15) reported that
when interventions were matched for carbohydrate and the
addition of protein resulted in greater energy content (i.e.,
nonisocaloric), CHO-PRO increased glycogen synthesis com-
pared with CHO. In the same study, when interventions were
matched for energy content (i.e., isocaloric), glycogen synthe-
sis was similar between CHO-PRO and CHO (15). However,
in a subsequent study by Howarth et al. (13), postexercise gly-
cogen synthesis was similar between CHO-PRO and CHO re-
gardless if interventions were isocaloric or nonisocaloric. These
result may suggests that other factors beyond energy content
mightneedtobeconsideredwhenassessingtheinfluenceof
CHO-PRO on glycogen synthesis. One such factor is the rela-
tive (g·kg
1
body mass·h
1
) amount of carbohydrate con-
sumed in a CHO-PRO supplement (2,3,16). Specifically, the
additive effect of CHO-PRO on glycogen synthesis as compared
with CHO alone may only be evident when carbohydrate content
is <0.8 g·kg
1
h
1
(2,3). When CHO intakes are >0.8 g·kg
1
h
1
,
glycogen synthesis is already maximally stimulated, thereby ne-
gating any potential effect of added protein (2,3).
The objective of this systematic review and meta-analysis was
to aggregate results from multiple studies to characterize the ef-
fects of CHO-PRO on glycogen synthesis during recovery from
exercise compared with CHO alone. In addition, subgroup anal-
yses were performed to examine if energy content (isocaloric and
nonisocaloric) or carbohydrate content modulates the effects of
CHO-PRO and CHO on glycogen synthesis. We hypothesized
that there would be no overall significant effect in postexercise
glycogen synthesis in CHO-PRO compared with CHO. We
further hypothesized that subgroup analysis would identify in-
creased postexercise glycogen synthesis with higher energy con-
tent (i.e., nonisocaloric) in CHO-PRO compared with PRO.
METHODS
Literature search strategy. Publication abstracts identi-
fied in PubMed (http://www.ncbi.nlm.nih.gov/pubmed) and
the Cochrane Library (https://www.cochranelibrary.com) were
organized using the Abstrackr citation program (http://
abstrackr.cebm.brown.edu) and reviewed for relevance by re-
searchers (JTA, AHM, and LMM). The initial search took place
on July 12, 2019, and was not restricted by publication date (see
Table, Supplemental Digital Content 1, Search terms used to
identify relevant articles, http://links.lww.com/MSS/C94). A
second search was conducted on March 24, 2020, to assess if
any new relevant manuscripts had been published since the first
search was performed. No new articles were identified. The Pre-
ferred Reporting Items for Systematic Reviews and Meta-analyses
(PRISMA) search strategy and further reference narrowing is
described in Figure 1 (17). The population, intervention, con-
trol, and outcome for this meta-analysis were healthy, trained
or untrained men or women, CHO-PRO, CHO only, and gly-
cogen synthesis, respectively. Reference lists from these pub-
lications were hand searched for relevant manuscripts missed
in the database search. One relevant manuscript (9) was iden-
tified. There were no language restrictions although English
search terms were used. Publications were reviewed and data
were extracted by two researchers (JTA and AHM). The final
decision on manuscript inclusion was conducted by LMM.
Inclusion criteria. Randomized and nonrandomized cross-
over controlled trials assessing the effect of CHO-PRO and
CHO on postexercise muscle glycogen synthesis in healthy,
trained or untrained men or women were included.
Exclusion criteria. Studies were excluded if there was no
exercise or recovery component, if there was no CHO-only
group, or if both groups consumed protein after exercise. Stud-
ies comparing CHO-PRO to CHO for outcomes other than
muscle glycogen synthesis were excluded. To control heteroge-
neity across studies, parallel study designs were excluded (18).
Bias and limitations. Bias was assessed by LMM in ac-
cordance with PRISMA guidelines recommended by Sterne
et al. (19). Ratings including low, some, or high concern of
randomization, intervention, outcomes, and reporting bias were
assigned to each study (see Table, Supplementary Digital Con-
tent 2, Risk of bias for publications included in the meta-
analysis, http://links.lww.com/MSS/C95).
Data extraction. Data were extracted from 20 articles that
met the inclusion and exclusion criteria (915,2032). Three
studies (9,13,15) had multiple groups, comparing isocaloric
and nonisocaloric interventions. Each intervention was treated
as an independent group. The final data extraction was con-
ducted on 23 groups. Sex, age, weight, V
˙
O
2max
, and training
status were extracted to provide volunteer descriptive charac-
teristics. Muscle glycogen measurements were extracted from
each study. Energy, carbohydrate, and protein intake from study
interventions were extracted. Data that were not presented
FIGURE 1PRISMA meta-regression search strategy diagram.
PROTEIN/CARBOHYDRATE AND MUSCLE GLYCOGEN Medicine & Science in Sports & Exercise
®
385
APPLIED SCIENCES
numerically were obtained using an image analysis software
(Image J, version 1.52a; National Institutes of Health, Bethesda,
MD) by digitally measuring the height of data points and
error bars and calculating relative to measured y-axis units
in histograms.
Statistical analysis. Meta-Essentials by van Rhee et al.
(33) with Microsoft Excel 2010 (Microsoft Corp., Redmond,
WA) was used to conduct the meta-analysis. Effect sizes
(ES) for the difference in delta (recovery minus immediately
postexercise) glycogen synthesis were determined as standard
mean difference between CHO-PRO and CHO divided by the
pooled standard deviation. Sample sizes, glycogen mean and
SD, and a correlation coefficient (r) for within-participant
measurements were imputed. Because of a lack of individual
data presented in publications, a correlation coefficient of
r= 0.80 generated from muscle glycogen data by our labora-
tory (34) was used across all studies. To confirm that outcomes
were not the result of our selection of r= 0.80, sensitivity anal-
ysis was conducted imputing an rvalue at a low of 0.50 and
high of 0.90. There was no difference in our results based on
the select rvalue. As such, all ES data were calculated using
r= 0.80. To account for heterogeneity, random effects were
applied and ES were generated as Hedgesg(35). To deter-
mine heterogeneity, both Qand I
2
statistics were used to assess
between-study variations in ES (35). Publication bias was de-
termined using the Egger regression (36). Subgroup analysis
was conducted to assess the influence of energy content (iso-
caloric and nonisocaloric) on postexercise glycogen synthesis.
Additional subgroup analysis was performed using median in-
take across studies to dichotomize carbohydrate content (high,
0.8 g·kg
1
h
1
;low,<0.8g·kg
1
h
1
). Glycogen data are pre-
sented as ES (95% confidence intervals [CI]). To confirm re-
sults of subgroup analysis, regression analysis was performed
with ES as the dependent variable and isocaloric or noniso-
caloric energy content, low or high carbohydrate content, rel-
ative carbohydrate intake (g·kg
1
h
1
), and relative protein
intake (g·kg
1
h
1
) as independent variables. In addition,
chi-square analysis was used, setting categories as significant
increase in glycogen synthesis (yes or no) and energy content
(isocaloric or nonisocaloric) or carbohydrate intake (high or
low) as categorical data using IBM SPSS Statistics for Windows
Version 26.0 (IBM Corp., Armonk, NY). All other data are pre-
sented as mean values. Statistical significance was set at P< 0.05.
RESULTS
Study characteristics. A total of 767 studies were iden-
tified and screened for inclusion (Fig. 1). Of these studies, 20
met the inclusion criteria, and within these 20 studies, 176 in-
dividuals participated (158 men and 18 women) (see Table,
Supplemental Digital Content 3, Volunteer characteristics,
http://links.lww.com/MSS/C96). For subgroup analysis, 23
groups were identified, with 10 groups ingesting isocaloric in-
terventions (Table 1) and 13 ingesting nonisocaloric interven-
tions (Table 2). Energy, carbohydrate, and protein intake for
subgroup analyses are presented in Table 3.
Glycogen synthesis. Overall, CHO-PRO had no signifi-
cant effect (0.13, 95% CI = 0.04 to 0.29) on glycogen synthesis
during recovery from exercise compared with CHO. There was
substantial (Q= 76, I
2
= 71%) heterogeneity across all studies.
In subgroup analysis for energy content, CHO-PRO had a pos-
itive effect (0.26, 95% CI = 0.040.49) on glycogen synthesis
when the energy content in CHO-PRO was higher (nonisocaloric)
than CHO (Fig. 2). When the energy content (isocaloric) was
matched, there was no significant effect in CHO-PRO (0.05,
95% CI = 0.23 to 0.13) compared with CHO (Fig. 2). There
was substantial heterogeneity in nonisocaloric studies (Q=47,
I
2
= 74%) and moderate heterogeneity in isocaloric studies
(Q=18,I
2
= 50%). In subgroup analysis for carbohydrate con-
tent, there was no significant effect of CHO-PRO in high (0.07,
95% CI = 0.11 to 0.25) or low (0.21, 95% CI = 0.08 to 0.50)
carbohydrate content compared with CHO (Fig. 3). Substantial
heterogeneity was detected in high (Q=31,I
2
= 61%) and low
(Q=44,I
2
= 80%) carbohydrate content studies.
Regression analysis identified energy content (isocaloric or
isocaloric) as a significant (P= 0.03) independent variable
explaining 17% (r
2
= 0.174) of the variance in glycogen syn-
thesis ES. Carbohydrate content (low or high), relative carbo-
hydrate intake, and relative protein intake were not significant
in the regression analysis model. Similarly, chi-square analysis
was significant (P= 0.03) when categorizing significant in-
crease in glycogen synthesis (yes or no) and energy content
(isocaloric or nonisocaloric). Chi-square analysis was not sig-
nificant when categorizing significant increase in glycogen
synthesis (yes or no) and carbohydrate content (high or low).
Publication bias. Publication bias was identified (P= 0.03)
in the 23 groups included in this meta-analysis (see Figure, Sup-
plemental Digital Content 4, Funnel plots of publication bias,
http://links.lww.com/MSS/C97). No publication bias was identi-
fied (P= 0.35) in assessing isocaloric studies alone. Publication
bias was identified (P= 0.03) when assessing nonisocaloric stud-
ies alone. Publication bias was driven by positive effects reported
in multiple studies (911,15). No publication bias was identified
in the overall data set (P= 0.81) or nonisocaloric subgroup
(P= 0.85) when these studies were removed from the data set.
However, there did not appear to be any inherit experimental or
methodological flaws to warrant exclusion of these studies from
the current investigation. Rather publication bias appeared to be
the result of studies reporting only positive or null effects, with
no studies reporting negative effects. As such, these investiga-
tions were included in the final analysis.
DISCUSSION
The primary outcome of this meta-analysis was that coingestion
of CHO-PRO had no overall significant effect on postexercise
glycogen synthesis compared with CHO alone. When studies
were dichotomized into high or low relative carbohydrate
intake, CHO-PRO had no significant effect on glycogen
synthesis compared with CHO. However, postexercise glyco-
gen synthesis was enhanced when the combined CHO-PRO
treatment provided more total energy than CHO alone. These
http://www.acsm-msse.org386 Official Journal of the American College of Sports Medicine
APPLIED SCIENCES
TABLE 1. Study design for isocaloric interventions.
Study Sample Size (n) Exercise Type
Exercise
Time (min)
Recovery
Time (h) Treatment Energy (kcal) CHO (g) Pro (g)
CHO
(g·kg
1
h
1
)
Pro
(g·kg
1
h
1
)
Glycogen
Synthesis
Glycogen
Measurement Method
Alghannam et al. (20) 6 (5M, 1F) Treadmill running; Time to
exhaustion 70% V
˙
O
2max
82 4 CHO 1277 319.2 1.20 37.4
a
Plate assay, dry weight
CHO-PRO 1277 212.8 106.4 0.80 0.40 41.7
a
Carrithers et al. (23) 7 (7M) Cycle ergometry 70% V
˙
O
2max
;sprint
to exhaustion
82.5 4 CHO 1206 301.6 1.00 31
a
Plate assay, dry weight
CHO-PRO 1206 259.3 42.2 0.86 0.14 28
a
Cogan et al. (12) 11 (11M) Cycle ergometry 70% V
˙
O
2max
120 4 CHO 720 180 0.60 0.58
b
Plate assay, wet weight
CHO-PRO 720 156 24 0.52 0.08 0.52
b
Detko et al. (24) 7 (7M) Intermittent cycle ergometry; 70%
and 120% V
˙
O
2max
120 4 CHO 1516 379 1.20 5.8
c
Magnetic resonance
spectroscopyCHO-PRO 1516 253 126 0.80 0.40 3.7
c
Ferguson-Stegall et al. (25) 10 (5M, 5F) Cycle ergometry 70% V
˙
O
2max
;
intervals 45% and 90% V
˙
O
2max
100 4 CHO 949 181.8 0.67 30.6
d
Plate assay, wet weight
CHO-PRO 949 137.8 44 0.51 0.16 23.9
d
Howarth et al. (13) 6 (6M) Intermittent cycle ergometer;
50%80% V
˙
O
2max
120 4 CHO 1728 432 1.20 25
a
Plate assay, dry weight
CHO-PRO 1728 324 108 0.90 0.30 25
a
Ivy et al. (9) 7 (7M) Cycle ergometry 65%75% V
˙
O
2max
;
sprint to exhaustion
150 4 CHO 640 160 0.54 8.4
c
Magnetic resonance
spectroscopyCHO-PRO 864 160 56 0.54 0.19 12.0
c
Lunn et al. (28) 6 (6M) Treadmill running 65% V
˙
O
2max
45 3 CHO 296 74 0.32 0.1
e
Plate assay, wet weight
CHO-PRO 296 58 16 0.25 0.07 0
e
Roy et al. (29) 10 (10M) Whole-body resistance exercise:
9 exercises/3 sets 80% 1RM
NR 4.5 CHO 694 173.6 0.44 19.3
a
Plate assay, dry weight
CHO-PRO 694 114.5 40 0.29 0.10 23.0
a
van Loon et al. (15) 8 (8M) Intermittent cycle ergometer;
50%90% V
˙
O
2max
100 5 CHO 1680 420 1.20 44.8
a
Plate assay, dry weight
CHO-PRO 1680 280 140 0.80 0.40 35.4
a
Values are presented as mean.
a
mmol·kg
1
muscle dry weight·h
1
.
b
μg·mg
1
muscle wet weight·h
1
.
c
mmol·L
1
·h
1
.
d
μmol·g
1
muscle wet weight·h
1
.
e
g per 100 g wet muscle weight·h
1
.
M, males; F, females.
PROTEIN/CARBOHYDRATE AND MUSCLE GLYCOGEN Medicine & Science in Sports & Exercise
®
387
APPLIED SCIENCES
TABLE 2. Study design for nonisocaloric interventions.
Study Sample Size (n) Exercise Type
Exercise
Time (min)
Recovery
Time (h) Treatment Energy (kcal) CHO (g) Pro (g)
CHO
(g·kg
1
h
1
)
Pro
(g·kg
1
h
1
)
Glycogen
Synthesis
Glycogen
Measurement Method
Beelen et al. (21) 14 (14M) Intermittent cycle ergometer;
50%90% V
˙
O
2max
106 4 CHO 2062 515.5 1.80 31
a
Plate assay, dry weight
CHO-PRO 2578 515.5 128.9 1.80 0.45 34
a
Betts et al. (22) 6 (6M) Treadmill running; 70% V
˙
O
2max
90 4 CHO 945 236.2 0.80 12.3
a
Plate assay, dry weight
CHO-PRO 1299 236.2 88.6 0.80 0.30 12.1
a
Howarth et al. (13) 6 (6M) Intermittent cycle ergometer;
50%80% V
˙
O
2max
120 4 CHO 1296 324 0.90 23
a
Plate assay, dry weight
CHO-PRO 1728 324 108 0.90 0.30 25
a
Ivy et al. (9) 7 (7M) Cycle ergometry 70% V
˙
O
2max
;
sprint to exhaustion
150 4 CHO 864 216 0.73 7.3
b
Magnetic resonance
spectroscopyCHO-PRO 864 160 56 0.54 0.19 12.0
b
Jentjens et al. (26) 8 (8M) Intermittent cycle ergometer
50%90% V
˙
O
2max
135 3 CHO 1002 250.6 1.20 40
a
Plate assay, dry weight
CHO-PRO 1336 250.6 83.5 1.20 0.40 25
a
Kammer et al. (27) 12 (8M, 4F) Cycle ergometry 60%65% V
˙
O
2max
120 2 CHO 314 78.5 1.10 6.2
c
Plate assay, wet weight
CHO-PRO 410 77 19.5 1.08 0.27 7.3
c
Tarnopolsky et al. (30) 16 (8M, 8F) Cycle ergometry 65% V
˙
O
2max
90 4 CHO 536 134 0.50 37.2
a
Plate assay, dry weight
CHO-PRO 480 100.5 13.4 0.38 0.05 24.6
a
van Loon et al. (8) 8 (8M) Intermittent cycle ergometer;
50%90% V
˙
O
2max
100 5 CHO 1120 280 0.80 16.4
a
Plate assay, dry weight
CHO-PRO 1680 280 140 0.80 0.40 35.4
a
Van Hall et al. (14) 5 (5M) Intermittent cycle ergometer
50%90% V
˙
O
2max
NR 4 CHO 492 123 0.42 39.8
a
Plate assay, dry weight
CHO-PRO 640 123 37 0.42 0.13 36.5
a
Van Hall et al. (31) 8 (8M) Intermittent cycle ergometer
50%90% V
˙
O
2max
NR 3 CHO 692 173 0.80 28.0
a
Plate assay, dry weight
CHO-PRO 952 173 65 0.80 0.30 34.0
a
Williams et al. (10) 8 (8M) Intermittent cycle ergometer
65%85% V
˙
O
2max
120 4 CHO 168 42 0.16 17.3
a
Plate assay, dry weight
CHO-PRO 536 106 28 0.39 0.10 39.8
a
Yaspelkis et al. (32) 12 (12M) Intermittent cycle ergometer
50%80% V
˙
O
2max
120 3 CHO 864 216 1.00 6.0
c
Plate assay, wet weight
CHO-PRO 933 216 17.3 1.00 0.08 8.2
c
Zawadzki et al. (11) 9 (9M) Intermittent cycle ergometer
50%85% V
˙
O
2max
120 4 CHO 896 224 0.77 26.7
d
Plate assay, wet weight
CHO-PRO 1222 224 81.4 0.77 0.28 35.5
d
Values are presented as mean.
a
mmol·kg
1
muscle dry weight·h
1
.
b
mmol·L
1
·h
1
.
c
μmol·g
1
muscle wet weight·h
1
.
d
μmol·g
1
muscle protein concentration.
M, males; F, females.
http://www.acsm-msse.org388 Official Journal of the American College of Sports Medicine
APPLIED SCIENCES
data indicate that increasing the energy content of postexercise
nutrition by adding protein to carbohydrate, and not replacing
carbohydrate for protein, is likely a primary stimulus for
enhanced glycogen synthesis during recovery from exercise
when CHO-PRO are consumed together.
Our meta-analysis demonstrated a significant positive effect
of combined CHO-PRO ingestion when the treatment provided
more energy than CHO alone. Our findings are in agreement
with van Loon et al. (15), who assessed postexercise glycogen
synthesis in individuals consuming 0.8 g CHO·kg
1
h
1
(low CHO), 1.2 g CHO·kg
1
h
1
(high CHO), or 0.8 g
CHO·kg
1
h
1
+ 0.4 g PRO·kg
1
h
1
(CHO-PRO). In the
study of van Loon et al. (15), postexercise glycogen synthesis
was greater after ingesting CHO-PRO compared with low CHO
(nonisocaloric comparison), but not different than high CHO
(isocaloric comparison). The authors suggested that the greater
glycogen synthesis rates observed after ingesting CHO-PRO
compared with the lower energy low CHO treatment was due
to an 88% higher postprandial insulin response (15). The
greater insulin response with CHO-PRO would, in theory,
enhance GLUT4 translocation, glucose uptake, and glycogen
synthase activity (15,37). Although van Loon et al. did not
explore these mechanisms, data from small animal studies
support this hypothesis and show that amino acids alone can
increase AKT and AS160 phosphorylation status, which are up-
stream regulators of GLUT4 translocation (38,39). However,
no studies have clearly delineated the mechanistic effects of
the additional energy content in combined CHO-PRO ingestion
from the potential insulinotropic effects provided by protein. The
study of van Loon et al. and our aggregate results do show that
when CHO-PRO and CHO are matched for total energy, there
is no direct benefit of displacing carbohydrate for protein.
By contrast, adding protein to matched amounts of carbohy-
drate will enhance glycogen synthesis.
FIGURE 2Values are presented as ES (95% CI) stratified by energy content.
TABLE 3. Energy, protein, and carbohydrate intake for subgroup analysis.
Subgroup Treatment Energy (kcals) Carbohydrate (g) Protein (g) Carbohydrate (g·kg
1
h
1
) Protein (g·kg
1
h
1
)
Isocaloric CHO 1093 ± 469 268 ± 120 0.86 ± 0.34
CHO-PRO 1093±469 195±84 70±45 0.63±0.24 0.22±0.14
Nonisocaloric CHO 848 ± 485 212 ± 121 0.84 ± 0.41
CHO-PRO 1128 ± 613 214 ± 117 67 ± 43 0.85 ± 0.39 0.26 ± 0.14
High carbohydrate CHO 1208 ± 483 302 ± 117 1.10 ± 0.27
CHO-PRO 1409 ± 519 262 ± 100 90 ± 43 0.98 ± 0.28 0.33 ± 0.12
Low carbohydrate CHO 625 ± 256 151 ± 59 0.52 ± 0.19
CHO-PRO 727±263 134±45 40±21 0.46±0.15 0.24±0.14
Values are presented as mean ± SD. High carbohydrate, 0.8 g·kg
1
h
1
; low carbohydrate, <0.8 g·kg
1
h
1
.
PROTEIN/CARBOHYDRATE AND MUSCLE GLYCOGEN Medicine & Science in Sports & Exercise
®
389
APPLIED SCIENCES
Dichotomizing studies by high (0.8 g·kg
1
h
1
)orlow
(<0.8 g·kg
1
h
1
) relative carbohydrate intake in the current
meta-analysis had no significant effect on glycogen synthe-
sis in CHO-PRO compared with CHO. This result appears
to contradict previous assertions that insulinotropic effects
of dietary protein may only be observed when postexercise
carbohydrate intake is <0.8 g·kg
1
h
1
(2,3). However, our
analysis may not definitively rule out an improvement in
glycogen synthesis when coingestion of protein occurs with
lower relative carbohydrate intake. Because of a limited
number of studies, we could not conduct subgroup analysis
on high and low relative carbohydrate intake between isoca-
loric and nonisocaloric studies. Similarly, there is no indi-
vidual study that has used a multigroup approach to assess
the effect of CHO-PRO compared with CHO using high
and low carbohydrate with isocaloric and nonisocaloric in-
terventions. Furthermore, although not statistically signifi-
cant, the ES was higher in low (0.21) compared with
high (0.07) relative carbohydrate subgroups, suggesting
that there may be some benefit of CHO-PRO on glycogen
synthesis when carbohydrate intake is <0.8 g·kg
1
h
1
.
Further investigation is needed to gain an understanding
how manipulating both carbohydrate and energy intake
(highenergy[highCHO+PRO,lowCHO+PRO];lowen-
ergy [high CHO + PRO, low CHO + PRO]) affects muscle gly-
cogen synthesis.
Moderate to substantial levels of heterogeneity were observed
across studies in the overall and subgroup analysis. Heteroge-
neity between studies is common and unavoidable with most
meta-analysis (40). Differences in exercise mode (running vs
cycling vs whole-body resistance exercise), assessment of muscle
glycogen (dry muscle mass vs wet muscle mass vs
13
C-magnetic
resonance spectroscopy), carbohydrate and protein sources, post-
exercise recovery duration, and timing of supplement intake
may have contributed to the observed heterogeneity. Subgroup
analysis identified that the use of isocaloric versus nonisocaloric
interventions resulted in different ES, suggesting that the differ-
ences in study interventions explain some degree of the overall
variance between studies. In addition, caution should be taken
when high levels of heterogeneity are detected if the direction
of individual study ES (e.g., positive or negative) vary across
studies and/or when individual CI do not overlap. Given that
all studies included in the current meta-analysis reported a
null or positive effect of CHO-PRO compared with CHO and
that the majority of CI overlapped between studies, it is un-
likely that the level of variance interfered with the present results
and interpretations.
Although consuming isocaloric CHO-PRO and CHO pro-
moted the same glycogen synthesis rates in recovery from ex-
ercise, a secondary advantage of coingesting carbohydrate and
protein, which is often overlooked in the context of aerobic ex-
ercise, is the primary effects of protein on muscle protein
FIGURE 3Values are presented as ES (95% CI) stratified by median relative carbohydrate content (high carbohydrate, 0.8 g·kg
1
h
1
; low carboh y-
drate, <0.8 g·kg
1
h
1
).
http://www.acsm-msse.org390 Official Journal of the American College of Sports Medicine
APPLIED SCIENCES
synthesis (41). There is no debate that increases in extracellu-
lar and intracellular amino acids when consuming CHO-PRO
postexercise increases muscle protein synthesis to a greater
extent than CHO (13,28). The fact that lower carbohydrate
intake with isocaloric CHO-PRO does not impair postex-
ercise glycogen synthesis, and that ingesting PRO will in-
crease muscle protein synthesis, indicates that CHO-PRO can
produce improved overall muscle recovery (i.e., glycogen
synthesis, repair, remodeling, and protein accretion) from ex-
ercise compared with CHO alone. In the current study, similar
glycogen synthesis rates were achieved despite a ~30% lower
carbohydrate intake in CHO-PRO compared with CHO. In
the context of current recommendations to consume carbo-
hydrate at 1.2 g·kg
1
h
1
to replenish glycogen stores post-
exercise, the present analysis indicates that carbohydrate can
be consumed at 0.9 g·kg
1
h
1
and protein at 0.3 g·kg
1
h
1
.
Matching energy intake at 1.2 g·kg
1
h
1
with coingestion
of CHO-PRO ensures adequate glycogen synthesis and that
postexercise protein requirements (0.250.3 g protein per
kilogram per meal postexercise) (1) are met to optimize muscle
protein recovery.
The results of this meta-analysis should be interpreted in the
context of the population and environment in which data were
collected. The studies included in the current meta-analysis
were performed under well-controlled laboratory settings.
Failure to consider the environmental conditions under which
skeletal muscle recovers and the necessity for postexercise
fueling may limit the extension of our analysis. For example,
recovery in environmental extremes such as heat and cold re-
sults in reduced postexercise glycogen synthesis (42,43). In
addition, unacclimatized exposure to environmental condi-
tions, such as heat and high altitude, increase glycogenolysis
and decrease the use of exogenous carbohydrate for fuel dur-
ing aerobic exercise (44,45). These changes in postexercise
glycogen synthesis, glycogenolysis, and exogenous glucose
oxidation during and in recovery from exercise may affect
postexercise recovery nutritional needs. However, the effect
of CHO-PRO on glycogen synthesis postexercise under envi-
ronmental extremes, such as heat, cold, and high altitude, has
not been examined. In addition, individual studies were pri-
marily conducted using male participants. Some research has
indicated that substrate oxidation differs by sex, with women
oxidizing more fat and less carbohydrate compared with men
during aerobic exercise (4649). However, there appear to be
minimal differences between sex postexercise, with men and
women exhibiting similar rates of glycogen synthesis postexer-
cise (30,50). This may suggest similar response in men and
women to CHO-PRO on glycogen synthesis postexercise. It
should also be noted that these studies were primarily conducted
with participants in a fasted state. Glycogen oxidation during
exercise is lower in fed compared with fasted states and affects
the rate of postexercise glycogen synthesis (51). It is unclear if
consuming a meal before exercise would affect the influence
of CHO-PRO on postexercise glycogen synthesis. Future in-
vestigation is needed to assess the application of recovery nu-
trition prescriptions for how environment, sex, and feeding
state (fasted or fed) may alter response to CHO-PRO on post-
exercise glycogen synthesis.
Although outside the scope of the current meta-analysis, in-
creased glycogen synthesis with nonisocaloric CHO-PRO is
uncertain, as limited studies assess both muscle glycogen and
physical performance. In the current meta-analysis, Williams
et al. (10) was the only study using a nonisocaloric intervention
to assess both glycogen synthesis and physical performance,
reporting a 55% increase in time-to-exhaustion performance
immediately after the 4-h recovery period in CHO-PRO com-
pared with CHO. However, recent systematic reviews have
stated that there is no overall benefit to physical performance
when consuming CHO-PRO compared with CHO (52,53). It
should be noted that these systematic reviews included perfor-
mance after consumption of isocaloric and nonisocaloric
CHO-PRO compared with CHO. As isocaloric CHO-PRO sup-
plementation did not result in a significant increase in glycogen
synthesis postexercise compared with CHO in the current meta-
analysis, an ergogenic effect would not be anticipated. Similar
to glycogen synthesis, the consumption of protein at the ex-
pense of carbohydrate was not reported to result in a negative
effect on physical performance in past systematic reviews
(52,53). Again this suggests that some carbohydrate can be re-
placed with dietary protein postexercise to obtain the benefit
of protein on muscle mass.
CONCLUSION
In conclusion, results from this meta-analysis indicate that
postexercise glycogen synthesis is enhanced by a higher en-
ergy intake when coingesting CHO-PRO compared with the
same amount of CHO alone. Equally important is our observa-
tion that ingesting CHO-PRO did not impair muscle glycogen
synthesis when compared with an isocaloric amount of CHO
only. As such, we contend that matching the energy content
provided in current sport nutrition recommendations for opti-
mal glycogen recovery of 1.2 g·kg
1
h
1
by lowering carbohy-
drate (0.9 g·kg
1
h
1
) and adding back the equivalent amount
of protein (0.3 g·kg
1
h
1
) may yield the most complete post-
exercise recovery by not only maximizing glycogen synthesis
but also by stimulating muscle protein synthesis.
The authors acknowledge Dr. Andrew Young for his critical review of
this manuscript as well as the subjects and authors of the papers in-
cluded in this meta-analysis. The authors also acknowledge Mr. Phil
Niro for generating the figures for the manuscript.
This work was supported by the U.S. Army Medical Research and
Development Command.
The investigators adhered to the policies for protection of human
subjects as prescribed in Army Regulation 70-25, and the research
was conducted in adherence with the provisions of 32 CFR part 219.
The opinions or assertions contained herein are the private views of
the authors and are not to be construed as official or as reflecting the
views of the Army or the Department of Defense. Any citations of com-
mercial organizations and trade names in this report do not constitute
an official Department of the Army endorsement of approval of the
products or services of these organizations.
The resultsof the study are presented clearly, honestly, and without
fabrication, falsification, or inappropriate data manipulation. Results of
the present study do not constitute endorsement by the American Col-
lege of Sports Medicine.
PROTEIN/CARBOHYDRATE AND MUSCLE GLYCOGEN Medicine & Science in Sports & Exercise
®
391
APPLIED SCIENCES
REFERENCES
1. Thomas DT, Erdman KA, Burke LM. American College of Sports
Medicine Joint Position Statement: nutrition and athletic perfor-
mance. Med Sci Sports Exerc. 2016;48(3):54368.
2. Alghannam AF, Gonzalez JT, Betts JA. Restoration of muscle glyco-
gen and functional capacity: role of post-exercise carbohydrate and
protein co-ingestion. Nutrients. 2018;10(2).
3. Betts JA, Williams C. Short-term recovery from prolonged exercise:
exploring the potential for protein ingestion to accentuate the benefits
of carbohydrate supplements. Sports Med. 2010;40(11):94159.
4. Floyd JC Jr, Fajans SS, Conn JW, Knopf RF, Rull J. Stimulation of
insulin secretion by amino acids. J Clin Invest. 1966;45(9):1487502.
5. Floyd JC Jr, Fajans SS, Conn JW, Thiffault C, Knopf RF, Guntsche
E. Secretion of insulin induced by amino acids and glucose in diabe-
tes mellitus. J Clin Endocrinol Metab. 1968;28(2):26676.
6. Doi M, Yamaoka I, Nakayama M, Mochizuki S, Sugahara K,
Yoshizawa F. Isoleucine, a blood glucose-lowering amino acid, increases
glucose uptake in rat skeletal muscle in the absence of increases in
AMP-activated protein kinase activity. JNutr. 2005;135(9):21038.
7. Doi M, Yamaoka I, Nakayama M, Sugahara K, Yoshizawa F. Hypo-
glycemic effect of isoleucine involves increased muscle glucose
uptake and whole body glucose oxidation and decreased hepatic
gluconeogenesis. Am J Physiol Endocrinol Metab. 2007;292(6):
E168393.
8. Ivy JL, Ding Z, Hwang H, Cialdella-Kam LC, Morrison PJ. Post ex-
ercise carbohydrate-protein supplementation: phosphorylation of mus-
cle proteins involved in glycogen synthesis and protein translation.
Amino Acids. 2008;35(1):8997.
9. Ivy JL, Goforth HW Jr, Damon BM, McCauley TR, Parsons EC,
Price TB. Early postexercise muscle glycogen recovery is enhanced with
a carbohydrate-protein supplement. J Appl Physiol (1985). 2002;93(4):
133744.
10. Williams M, Raven PB, Fogt DL, Ivy JL. Effects of recovery bever-
ages on glycogen restoration and endurance exercise performance. J
Strength Cond Res. 2003;17(1):129.
11. Zawadzki KM, Yaspelkis BB 3rd, Ivy JL. Carbohydrateprotein
complex increases the rate of muscle glycogen storage after exercise.
J Appl Physiol (1985). 1992;72(5):18549.
12. Cogan KE, Evans M, Iuliano E, et al. Co-ingestion of protein or a
protein hydrolysate with carbohydrate enhances anabolic signaling,
but not glycogen resynthesis, following recovery from prolonged aerobic
exercise in trained cyclists. Eur J Appl Physiol. 2018;118(2):34959.
13. Howarth KR, Moreau NA, Phillips SM, Gibala MJ. Coingestion of
protein with carbohydrate during recovery from endurance exercise
stimulates skeletal muscle protein synthesis in humans. J Appl Phys-
iol (1985). 2009;106(4):1394402.
14. van Hall G, Shirreffs SM, Calbet JA. Muscle glycogen resynthesis
during recovery from cycle exercise: no effect of additional protein
ingestion. J Appl Physiol (1985). 2000;88(5):16316.
15. van Loon LJ, Saris WH, Kruijshoop M, Wagenmakers AJ. Maximiz-
ing postexercise muscle glycogen synthesis: carbohydrate supple-
mentation and the application of amino acid or protein hydrolysate
mixtures. Am J Clin Nutr. 2000;72(1):10611.
16. Burke LM, van Loon LJC, Hawley JA. Postexercise muscle glycogen
resynthesis in humans. J Appl Physiol (1985). 2017;122(5):105567.
17. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Pre-
ferred Reporting Items for Systematic Reviews and Meta-analyses:
the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
18. Cochrane Handbook for Systematic Reviews of Interventions.The
Cochrane Collaboration; 2011.
19. Sterne JAC, SavovićJ, Page MJ, et al. RoB 2: a revised tool for
assessing risk of bias in randomised trials. BMJ. 2019;366:l4898.
20. Alghannam AF, Jedrzejewski D, Bilzon J, Thompson D, Tsintzas K,
Betts JA. Influence of post-exercise carbohydrate-protein ingestion
on muscle glycogen metabolism in recovery and subsequent running
exercise. Int J Sport Nutr Exerc Metab. 2016;26(6):57280.
21. Beelen M, Kranenburg Jv, Senden JM, Kuipers H, Loon LJ. Impact
of caffeine and protein on postexercise muscle glycogen synthesis.
Med Sci Sports Exerc. 2012;44(4):692700.
22. Betts JA, Williams C, Boobis L, Tsintzas K. Increased carbohydrate
oxidation after ingesting carbohydrate with added protein. Med Sci
Sports Exerc. 2008;40(5):90312.
23. Carrithers JA, Williamson DL, Gallagher PM, Godard MP, Schulze
KE, Trappe SW. Effects of postexercise carbohydrate-protein feed-
ings on muscle glycogen restoration. J Appl Physiol (1985). 2000;
88(6):197682.
24. Detko E, OHara JP, Thelwall PE, et al. Liver and muscle glycogen
repletion using 13C magnetic resonance spectroscopy following in-
gestion of maltodextrin, galactose, protein and amino acids. Br J
Nutr. 2013;110(5):84855.
25. Ferguson-Stegall L, McCleave EL, Ding Z, et al. Postexercise
carbohydrate-protein supplementation improves subsequent exercise
performance and intracellular signaling for protein synthesis. JStrength
Cond Res. 2011;25(5):121024.
26. Jentjens RL, van Loon LJ, Mann CH, Wagenmakers AJ, Jeukendrup
AE. Addition of protein and amino acids to carbohydrates does not
enhance postexercise muscle glycogen synthesis. JApplPhysiol
(1985). 2001;91(2):83946.
27. Kammer L, Ding Z, Wang B, Hara D, Liao YH, Ivy JL. Cereal and
nonfat milk support muscle recovery following exercise. J Int Soc
Sports Nutr. 2009;6:11.
28. Lunn WR, Pasiakos SM, Colletto MR, et al. Chocolate milk and en-
durance exercise recovery: protein balance, glycogen, and perfor-
mance. Med Sci Sports Exerc. 2012;44(4):68291.
29. Roy BD, Tarnopolsky MA. Influence of differing macronutrient in-
takes on muscle glycogenresynthesis after resistance exercise. J Appl
Physiol (1985). 1998;84(3):8906.
30. Tarnopolsky MA, Bosman M, Macdonald JR, Vandeputte D, Martin
J, Roy BD. Postexercise protein-carbohydrate and carbohydrate sup-
plements increase muscle glycogen in men and women. J Appl Phys-
iol (1985). 1997;83(6):187783.
31. van Hall G, Saris WH, van de Schoor PA, Wagenmakers AJ. The ef-
fect of free glutamine and peptide ingestion on the rate ofmuscle gly-
cogen resynthesis in man. Int J Sports Med. 2000;21(1):2530.
32. Yaspelkis BB 3rd, Ivy JL. The effect of a carbohydratearginine sup-
plement on postexercise carbohydrate metabolism. Int J Sport Nutr.
1999;9(3):24150.
33. van Rhee HJ. User Manual for Meta-Essentials: Workbooks for
Meta-analysis. Rotterdam (The Netherlands): Erasmus Research Insti-
tute of Management; 2015. Available from: Erasmus Research Institute
of Management.
34. Margolis LM, Wilson MA, Whitney CC, et al. Exercising with low
muscle glycogen content increases fat oxidation and decreases en-
dogenous, but not exogenous carbohydrate oxidation. Metabolism.
2019;97:18.
35. Borenstein M, Hedges LV, Higgins JPT. Introduction to Meta-
Analysis. Chichester (UK): John Wiley & Sons; 2009.
36. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis
detected by a simple, graphical test. BMJ. 1997;315(7109):62934.
37. Ivy JL, Kuo CH. Regulation of GLUT4 protein and glycogen syn-
thase during muscle glycogen synthesis after exercise. Acta Physiol
Scand. 1998;162(3):295304.
38. Bernard JR, Liao YH, Ding Z, et al. An amino acid mixture improves
glucose tolerance and lowers insulin resistance in the obese Zucker
rat. Amino Acids. 2013;45(1):191203.
39. Kleinert M, Liao YH, Nelson JL, Bernard JR, Wang W, Ivy JL. An
amino acid mixture enhances insulin-stimulated glucose uptake
in isolated rat epitrochlearis muscle. J Appl Physiol (1985). 2011;
111(1):1639.
40. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring incon-
sistency in meta-analyses. BMJ. 2003;327(7414):55760.
http://www.acsm-msse.org392 Official Journal of the American College of Sports Medicine
APPLIED SCIENCES
41. Margolis LM, Pasiakos SM. Optimizing intramuscular adaptations to
aerobic exercise: effects of carbohydrate restriction and protein
su pp lem en tat io n on mitochondrial biogenesis. Adv Nutr. 2013;4(6):
65764.
42. Tucker TJ, Slivka DR, Cuddy JS, Hailes WS, Ruby BC. Effect of lo-
cal cold application on glycogen recovery. J Sports Med Phys Fit-
ness. 2012;52(2):15864.
43. Naperalsky M, Ruby B, Slivka D. Environmental temperature and
glycogen resynthesis. Int J Sports Med. 2010;31(8):5616.
44. Jentjens RL, Wagenmakers AJ, Jeukendrup AE. Heatstress increases
muscle glycogen use but reduces the oxidation of ingested carbohy-
drates during exercise. J Appl Physiol (1985). 2002;92(4):156272.
45. Margolis LM, Wilson MA, Whitney CC, et al. Acute hypoxia re-
duces exogenous glucose oxidation, glucose turnover, and metabolic
clearance rate during steady-state aerobic exercise. Metabolism. 2019;
103:154030.
46. Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during
endurance exercise in men and women after endurance training. Am
J Physiol Endocrinol Metab. 2001;280(6):E898907.
47. Devries MC, Hamadeh MJ, Phillips SM, Tarnopolsky MA. Men-
strual cycle phase and sex influence muscle glycogen utilization
and glucose turnover during moderate-intensity endurance exercise.
Am J Physiol Regul Integr Comp Physiol. 2006;291(4):R11208.
48. Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky
SN, Devries MC, Hamadeh MJ. Influence of endurance exercise
training and sex on intramyocellular lipid and mitochondrial ultra-
structure, substrate use, and mitochondrial enzyme activity. Am J
Physiol Regul Integr Comp Physiol. 2007;292(3):R12718.
49. Tarnopolsky MA, Atkinson SA, Phillips SM, MacDougall JD. Car-
bohydrate loading and metabolism during exercise in men and women.
J Appl Physiol (1985). 1995;78(4):13608.
50. Flynn S, Rosales A, Hailes W, Ruby B. Males and females exhibit
similar muscle glycogen recovery with varied recovery food sources.
Eur J Appl Physiol. 2020;120(5):113142.
51. De Bock K, Richter EA, Russell AP, et al. Exercise in the fasted state
facilitates fibre type-specific intramyocellular lipid breakdown and
stimulates glycogen resynthesis in humans. J Physiol. 2005;564(Pt 2):
64960.
52. McCartney D, Desbrow B, Irwin C. Post-exercise ingestion of carbo-
hydrate, protein and water: a systematic review and meta-analysis for
effects on subsequent athletic performance. Sports Med. 2018;48(2):
379408.
53. McLellan TM, Pasiakos SM, Lieberman HR. Effects of protein in
combination with carbohydrate supplements on acute or repeat endur-
ance exercise performance: a systematic review. Sports Med. 2014;
44(4):53550.
PROTEIN/CARBOHYDRATE AND MUSCLE GLYCOGEN Medicine & Science in Sports & Exercise
®
393
APPLIED SCIENCES
... This finding was preserved when contextual factors were explored using metaregression analysis (Table 4). It is also consistent with results from previous meta-analyses indicating that coingestion of PRO with CHO during short-term recovery does not improve short-term muscle glycogen resynthesis [67] or subsequent exercise performance [68]. ...
... A recent meta-analysis [67] similar to the present study reported a significant main effect (favouring CHO+PRO over CHO) on muscle glycogen re-synthesis rate when the energy intake was not matched between treatments (non-isocaloric). This finding contrasts the results of the present study ( Table 4). ...
... The discrepancy between findings may be due to a number of factors. Firstly, different effect estimates were used between studies; we reported the mean difference for ease of interpretation [70], whereas Margolis et al. [67] reported Hedges' g. Secondly, studies employing 13 C-MRS techniques to determine muscle glycogen concentration were included in the previous study, while our results are based on studies using muscle tissue samples for glycogen analysis (as a means of reducing methodological heterogeneity). ...
Article
Full-text available
Background Rapid restoration of muscle glycogen stores is imperative for athletes undertaking consecutive strenuous exercise sessions with limited recovery time (e.g. ≤ 8 h). Strategies to optimise muscle glycogen re-synthesis in this situation are essential. This two-part systematic review and meta-analysis investigated the effect of consuming carbohydrate (CHO) with and without protein (PRO) on the rate of muscle glycogen re-synthesis during short-term post-exercise recovery (≤ 8 h). Methods Studies were identified via the online databases Web of Science and Scopus. Investigations that measured muscle glycogen via needle biopsy during recovery (with the first measurement taken ≤ 30 min post-exercise and at least one additional measure taken ≤ 8 h post-exercise) following a standardised exercise bout (any type) under the following control vs. intervention conditions were included in the meta-analysis: part 1, water (or non-nutrient beverage) vs. CHO, and part 2, CHO vs. CHO+PRO. Publications were examined for methodological quality using the Rosendal scale. Random-effects meta-analyses and meta-regression analyses were conducted to evaluate intervention efficacy. Results Overall, 29 trials ( n = 246 participants) derived from 21 publications were included in this review. The quality assessment yielded a Rosendal score of 61 ± 8% (mean ± standard deviation). Part 1: 10 trials ( n = 86) were reviewed. Ingesting CHO during recovery (1.02 ± 0.4 g·kg body mass (BM) ⁻¹ h ⁻¹ ) improved the rate of muscle glycogen re-synthesis compared with water; change in muscle glycogen (MG Δ ) re-synthesis rate = 23.5 mmol·kg dm ⁻¹ h ⁻¹ , 95% CI 19.0–27.9, p < 0.001; I ² = 66.8%. A significant positive correlation ( R 2 = 0.44, p = 0.027) was observed between interval of CHO administration (≤ hourly vs. > hourly) and the mean difference in rate of re-synthesis between treatments. Part 2: 19 trials ( n = 160) were reviewed. Ingesting CHO+PRO (CHO: 0.86 ± 0.2 g·kg BM ⁻¹ h ⁻¹ ; PRO: 0.27 ± 0.1 g·kg BM ⁻¹ h ⁻¹ ) did not improve the rate of muscle glycogen re-synthesis compared to CHO alone (0.95 ± 0.3 g·kg BM ⁻¹ h ⁻¹ ); MG Δ re-synthesis rate = 0.4 mmol·kg dm ⁻¹ h ⁻¹ , 95% CI −2.7 to 3.4, p = 0.805; I ² = 56.4%. Conclusions Athletes with limited time for recovery between consecutive exercise sessions should prioritise regular intake of CHO, while co-ingesting PRO with CHO appears unlikely to enhance (or impede) the rate of muscle glycogen re-synthesis. Trial Registration Registered at the International Prospective Register of Systematic Reviews (PROSPERO) (identification code CRD42020156841 ).
... The relationship between postexercise carbohydrate (CHO) intake and subsequent endurance performance is well established, but equivocal evidence exists of the role of protein in the restoration of whole-body glycogen stores (Alghannam et al., 2018). Several studies have suggested that providing protein together with optimal CHO (1.2 g·kg −1 ·hr −1 ) does not further enhance short-term (<8 hr) glycogen restoration (Margolis et al., 2021). However, in endurance athletes' habitual eating practices, postexercise CHO intake often remains inadequate (Burke et al., 2003;Heikura et al., 2019;Keay et al., 2018); therefore, optimizing recovery meal composition may help to improve glycogen replenishment. ...
... In contrast to previous original investigations, we specifically asked whether athletes could benefit from acute addition of PRO or PROH to CHO after 24 hr (rather than 4-8 hr) of recovery if CHO intake is suboptimal. The results of three recent meta-analyses (Craven et al., 2021;Kloby Nielsen et al., 2020;Margolis et al., 2021) demonstrate that CHO+protein is effective in the short term (<8 hr) when energy intake is higher than CHO as a result of additional protein but not in isocaloric experiments. Suboptimal CHO may be where the positive effect of protein manifests itself, but the question remains whether this short-term benefit has relevance to real-world training of amateur athletes. ...
Article
Supplementing postexercise carbohydrate (CHO) intake with protein has been suggested to enhance recovery from endurance exercise. The aim of this study was to investigate whether adding protein to the recovery drink can improve 24-hr recovery when CHO intake is suboptimal. In a double-blind crossover design, 12 trained men performed three 2-day trials consisting of constant-load exercise to reduce glycogen on Day 1, followed by ingestion of a CHO drink (1.2 g·kg ⁻¹ ·2 hr ⁻¹ ) either without or with added whey protein concentrate (CHO + PRO) or whey protein hydrolysate (CHO + PROH) (0.3 g·kg ⁻¹ ·2 hr ⁻¹ ). Arterialized blood glucose and insulin responses were analyzed for 2 hr postingestion. Time-trial performance was measured the next day after another bout of glycogen-reducing exercise. The 30-min time-trial performance did not differ between the three trials ( M ± SD , 401 ± 75, 411 ± 80, 404 ± 58 kJ in CHO, CHO + PRO, and CHO + PROH, respectively, p = .83). No significant differences were found in glucose disposal (area under the curve [AUC]) between the postexercise conditions (364 ± 107, 341 ± 76, and 330 ± 147, mmol·L ⁻¹ ·2 hr ⁻¹ , respectively). Insulin AUC was lower in CHO (18.1 ± 7.7 nmol·L ⁻¹ ·2 hr ⁻¹ ) compared with CHO + PRO and CHO + PROH (24.6 ± 12.4 vs. 24.5 ± 10.6, p = .036 and .015). No difference in insulin AUC was found between CHO + PRO and CHO + PROH. Despite a higher acute insulin response, adding protein to a CHO-based recovery drink after a prolonged, high-intensity exercise bout did not change next-day exercise capacity when overall 24-hr macronutrient and caloric intake was controlled.
... We acknowledge that the collection of biopsy samples from adjacent, but non-identical sites, or sites from contra-lateral limbs in scenarios involving symmetrical exercise protocols, may contribute to the technical error of measurement involved with chemical determination of muscle glycogen stores. Nevertheless, it is the basis of a robust literature involving many hundreds of studies, which have determined resting muscle glycogen concentrations in different populations [36], glycogen utilisation during exercise [1,53], and glycogen synthesis in response to diet [19,54,55]. ...
Article
Full-text available
Researchers and practitioners in sports nutrition would greatly benefit from a rapid, portable, and non-invasive technique to measure muscle glycogen, both in the laboratory and field. This explains the interest in MuscleSound®, the first commercial system to use high-frequency ultrasound technology and image analysis from patented cloud-based software to estimate muscle glycogen content from the echogenicity of the ultrasound image. This technique is based largely on muscle water content, which is presumed to act as a proxy for glycogen. Despite the promise of early validation studies, newer studies from independent groups reported discrepant results, with MuscleSound® scores failing to correlate with the glycogen content of biopsy-derived mixed muscle samples or to show the expected changes in muscle glycogen associated with various diet and exercise strategies. The explanation of issues related to the site of assessment do not account for these discrepancies, and there are substantial problems with the premise that the ratio of glycogen to water in the muscle is constant. Although further studies investigating this technique are warranted, current evidence that MuscleSound® technology can provide valid and actionable information around muscle glycogen stores is at best equivocal.
... Therefore, milk protein is expected to both promote and sustain muscle protein synthesis. A recent meta-analysis reported that glycogen synthesis rates are enhanced when carbohydrates and protein are co-ingested after exercise compared to carbohydrates only, when the added energy of protein is consumed in addition to, not in place of, carbohydrates, suggesting the importance of an increase in the energy intake [64]. It is well known that modulating postexercise nutrition is an effective approach to enhance the replenishment of muscle glycogen stores. ...
Article
Full-text available
With the growing number of dialysis patients with frailty, the concept of renal rehabilitation, including exercise intervention and nutrition programs for patients with chronic kidney disease (CKD), has become popular recently. Renal rehabilitation is a comprehensive multidisciplinary program for CKD patients that is led by doctors, rehabilitation therapists, diet nutritionists, nursing specialists, social workers, pharmacists, and therapists. Many observational studies have observed better outcomes in CKD patients with more physical activity. Furthermore, recent systematic reviews have shown the beneficial effects of exercise intervention on exercise tolerance, physical ability, and quality of life in dialysis patients, though the beneficial effect on overall mortality remains unclear. Nutritional support is also fundamental to renal rehabilitation. There are various causes of skeletal muscle loss in CKD patients. To prevent muscle protein catabolism, in addition to exercise, a sufficient supply of energy, including carbohydrates, protein, iron, and vitamins, is needed. Because of decreased digestive function and energy loss due to dialysis treatment, dialysis patients are recommended to ingest 1.2-fold more protein than the regular population. Motivating patients to join in activities is also an important part of renal rehabilitation. It is essential for us to recognize the importance of renal rehabilitation to maximize patient satisfaction.
Article
Sarcopenic obesity is a new category of obesity and is a specific condition of sarcopenia. This study aimed to find the relationship of the basal metabolic rate (BMR) and body water distribution with muscle health and their prospective roles in screening for sarcopenic obesity and sarcopenia. The role of nutrients such as carbohydrates in the relationship was further detected. A total of 402 elderly subjects were recruited. Body composition was estimated by bioelectrical impedance analysis. Sarcopenia was defined by the Asian Working Group for Sarcopenia 2019. The cutoff values were determined by the receiver operating characteristic curve. Mediation analyses were performed using SPSS PROCESS. Higher BMR and BMR/body surface area (BSA) were protective factors against sarcopenic obesity (OR = 0.047, p = 0.004; OR = 0.035, p = 0.002) and sarcopenia (OR = 0.085, p = 0.001; OR = 0.100, p = 0.003) in elderly people. Low extracellular water (ECW)/intracellular water (ICW) and ECW/total body water (TBW) were negatively correlated with the skeletal muscle index (SMI). The intake of dietary carbohydrates in people with sarcopenic obesity was the lowest, but in subjects with obesity, it was the highest (p = 0.023). The results of the moderated mediation model showed that BMR fully mediated the positive relationship between carbohydrates and SMI, which was more obvious in the population with an abnormal body water distribution. BMR or BMR/BSA had the potential role of predicting a higher risk of sarcopenic obesity and sarcopenia. Higher BMR and lower ECW/ICW and ECW/TBW may benefit muscle health. The overconsumption of carbohydrates (especially > AMDR) might be a risk factor for obesity. Moderate dietary carbohydrate intake might promote SMI by regulating BMR and body water distribution in the elderly.
Article
Full-text available
Introduction: The addition of protein to a carbohydrate solution has been shown to effectively stimulate glycogen synthesis in an acute setting and enhance exercise performance in a subsequent bout of exhaustive exercise. This study examined the effects of carbohydrate-protein (CHO-P), carbohydrate (CHO), and placebo (PLA) within a 2-hour recovery period on subsequent high-intensity exercise performance. Methods: This was a randomized, single-blind between-subject design. Participants (n = 25) were assigned to consume one of three beverages during a 2-hour recovery period: PLA, CHO (1.2 g/kg bm), or CHO-P (0.8 g/kg bm CHO + 0.4 g/kg bm PRO). During Visit#1, participants completed graded exercise testing (VO2peak; cycle ergometer). Familiarization (Visit#2) consisted of 5 x 4 min intervals at 70-80% of peak power output [PPO, watts] with two minutes of active recovery at 50W, followed by time to exhaustion [TTE] at 90% PPO. The same high-intensity interval protocol with TTE was conducted pre-and post-beverage consumption on Visit #3. Results: The ANCOVA indicated a significant difference among the group means for the posttest TTE (F2,21=8.248, p=.002, ƞ2=.440) and RER (F2,21=6.811, p=.005, ƞ2=.393) values after adjusting for the pretest differences. Conclusions: Carbohydrate-protein co-ingestion was effective in promoting an increase in TTE performance with limited time to recover.
Article
Full-text available
PurposeResearch has elucidated the impact of post-exercise carbohydrate nutrition and environmental conditions on muscle glycogen re-synthesis. However, research has minimally considered the implications of glycogen recovery in females and has mostly focused on commercial sport nutrition products. The purpose of this study was to determine the effects of varied mixed macronutrient feedings on glycogen recovery and subsequent exercise performance in both sexes.Methods Males (n = 8) and females (n = 8) participated in a crossover study. Subjects completed a 90-min cycling glycogen depletion trial, then rested for 4 h. Two carbohydrate feedings (1.6 g kg−1) of either sport supplements or potato-based products were delivered at 0 and 2 h post-exercise. Muscle biopsies (glycogen) and blood samples (glucose, insulin) were collected during the recovery. Afterwards, subjects completed a 20 km cycling time trial.ResultsThere was no difference between sexes or trials for glycogen recovery rates (male: 7.9 ± 2.7, female: 8.2 ± 2.7, potato-based: 8.0 ± 2.5, sport supplement: 8.1 ± 3.1 mM kg wet wt−1 h−1, p > 0.05). Time trial performance was not different between diets (38.3 ± 4.4 and 37.8 ± 3.9 min for potato and sport supplement, respectively, p > 0.05).Conclusions These results indicate that food items, such as potato-based products, can be as effective as commercially marketed sports supplements when developing glycogen recovery oriented menus and that absolute carbohydrate dose feedings (g kg−1) can be effectively applied to both males and females.
Article
Full-text available
The importance of post-exercise recovery nutrition has been well described in recent years, leading to its incorporation as an integral part of training regimes in both athletes and active individuals. Muscle glycogen depletion during an initial prolonged exercise bout is a main factor in the onset of fatigue and so the replenishment of glycogen stores may be important for recovery of functional capacity. Nevertheless, nutritional considerations for optimal short-term (3–6 h) recovery remain incompletely elucidated, particularly surrounding the precise amount of specific types of nutrients required. Current nutritional guidelines to maximise muscle glycogen availability within limited recovery are provided under the assumption that similar fatigue mechanisms (i.e., muscle glycogen depletion) are involved during a repeated exercise bout. Indeed, recent data support the notion that muscle glycogen availability is a determinant of subsequent endurance capacity following limited recovery. Thus, carbohydrate ingestion can be utilised to influence the restoration of endurance capacity following exhaustive exercise. One strategy with the potential to accelerate muscle glycogen resynthesis and/or functional capacity beyond merely ingesting adequate carbohydrate is the co-ingestion of added protein. While numerous studies have been instigated, a consensus that is related to the influence of carbohydrate-protein ingestion in maximising muscle glycogen during short-term recovery and repeated exercise capacity has not been established. When considered collectively, carbohydrate intake during limited recovery appears to primarily determine muscle glycogen resynthesis and repeated exercise capacity. Thus, when the goal is to optimise repeated exercise capacity following short-term recovery, ingesting carbohydrate at an amount of ≥1.2 g kg body mass−1·h−1 can maximise muscle glycogen repletion. The addition of protein to carbohydrate during post-exercise recovery may be beneficial under circumstances when carbohydrate ingestion is sub-optimal (≤0.8 g kg body mass−1·h−1) for effective restoration of muscle glycogen and repeated exercise capacity.
Article
Full-text available
Purpose: The effect of carbohydrate (CHO), or CHO supplemented with either sodium caseinate protein (CHO-C) or a sodium caseinate protein hydrolysate (CHO-H) on the recovery of skeletal muscle glycogen and anabolic signaling following prolonged aerobic exercise was determined in trained male cyclists [n = 11, mean ± SEM age 28.8 ± 2.3 years; body mass (BM) 75.0 ± 2.3 kg; VO2peak 61.3 ± 1.6 ml kg-1 min-1]. Methods: On three separate occasions, participants cycled for 2 h at ~ 70% VO2peak followed by a 4-h recovery period. Isoenergetic drinks were consumed at + 0 and + 2 h of recovery containing either (1) CHO (1.2 g kg -1 BM), (2) CHO-C, or (3) CHO-H (1.04 and 0.16 g kg-1 BM, respectively) in a randomized, double-blind, cross-over design. Muscle biopsies from the vastus lateralis were taken prior to commencement of each trial, and at + 0 and + 4 h of recovery for determination of skeletal muscle glycogen, and intracellular signaling associated with protein synthesis. Results: Despite an augmented insulin response following CHO-H ingestion, there was no significant difference in skeletal muscle glycogen resynthesis following recovery between trials. CHO-C and CHO-H co-ingestion significantly increased phospho-mTOR Ser2448 and 4EBP1 Thr37/46 versus CHO, with CHO-H displaying the greatest change in phospho-4EBP1 Thr37/46. Protein co-ingestion, compared to CHO alone, during recovery did not augment glycogen resynthesis. Conclusion: Supplementing CHO with intact sodium caseinate or an insulinotropic hydrolysate derivative augmented intracellular signaling associated with skeletal muscle protein synthesis following prolonged aerobic exercise.
Article
Full-text available
Background Athletes may complete consecutive exercise sessions with limited recovery time between bouts (e.g. ≤ 4 h). Nutritional strategies that optimise post-exercise recovery in these situations are therefore important. Objective This two-part review investigated the effect of consuming carbohydrate (CHO) and protein with water (W) following exercise on subsequent athletic (endurance/anaerobic exercise) performance. Data SourcesStudies were identified by searching the online databases SPORTDiscus, PubMed, Web of Science and Scopus. Study Eligibility Criteria and InterventionsInvestigations that measured endurance performance (≥ 5 min duration) ≤ 4 h after a standardised exercise bout (any type) under the following control vs. intervention conditions were included: Part 1: W vs. CHO ingested with an equal volume of W (CHO + W); and, Part 2: CHO + W vs. protein (PRO) ingested with CHO and an equal volume of W (PRO + CHO + W), where CHO or energy intake was matched. Study Appraisal and Synthesis Methods Publications were examined for bias using the Rosendal scale. Random-effects meta-analyses and meta-regression analyses were conducted to evaluate intervention efficacy. ResultsThe quality assessment yielded a Rosendal score of 63 ± 9% (mean ± standard deviation). Part 1: 45 trials (n = 486) were reviewed. Ingesting CHO + W (102 ± 50 g CHO; 0.8 ± 0.6 g CHO kg−1 h−1) improved exercise performance compared with W (1.6 ± 0.7 L); %Δ mean power output = 4.0, 95% confidence interval 3.2–4.7 (I2 = 43.9). Improvement was attenuated when participants were ‘Fed’ (a meal 2–4 h prior to the initial bout) as opposed to ‘Fasted’ (p = 0.012). Part 2: 13 trials (n = 125) were reviewed. Ingesting PRO + CHO + W (35 ± 26 g PRO; 0.5 ± 0.4 g PRO kg−1) did not affect exercise performance compared with CHO + W (115 ± 61 g CHO; 0.6 ± 0.3 g CHO·kg body mass−1 h−1; 1.2 ± 0.6 L); %Δ mean power output = 0.5, 95% confidence interval − 0.5 to 1.6 (I2 = 72.9). Conclusions Athletes with limited time for recovery between consecutive exercise sessions should prioritise CHO and fluid ingestion to enhance subsequent athletic performance. PROSPERO Registration NumberCRD42016046807.
Article
Full-text available
Since the pioneering studies conducted in the 1960s in which glycogen status was investigated utilizing the muscle biopsy technique, sports scientists have developed a sophisticated appreciation of the role of glycogen in cellular adaptation and exercise performance, as well as sites of storage of this important metabolic fuel. While sports nutrition guidelines have evolved during the past decade to incorporate sport-specific and periodized manipulation of carbohydrate (CHO) availability, athletes attempt to maximise muscle glycogen synthesis between important workouts or competitive events so that fuel stores closely match to the demands of the prescribed exercise. Therefore, it is important to understand the factors that enhance or impair this biphasic process. In the early post-exercise period (0-4 h), glycogen depletion provides a strong drive for its own resynthesis, with the provision of carbohydrate (CHO; ~ 1 g/kg body mass [BM]) optimizing this process. During the later phase of recovery (4-24 h), CHO intake should meet the anticipated fuel needs of the training/competition, with the type, form and pattern of intake being less important than total intake. Dietary strategies that can enhance glycogen synthesis from sub-optimal amounts of CHO or energy intake are of practical interest to many athletes; in this scenario, the co-ingestion of protein with CHO can assist glycogen storage. Future research should identify other factors that enhance the rate of synthesis of glycogen storage in a limited time-frame, improve glycogen storage from a limited CHO intake or increase muscle glycogen supercompensation.
Article
Background: Exogenous carbohydrate oxidation is lower during steady-state aerobic exercise in native lowlanders sojourning at high altitude (HA) compared to sea level (SL). However, the underlying mechanism contributing to reduction in exogenous carbohydrate oxidation during steady-state aerobic exercise performed at HA have not been explored. Objective: To determine if alterations in glucose rate of appearance (Ra), disappearance (Rd) and metabolic clearance rate (MCR) at HA provide a mechanism for explaining the observation of lower exogenous carbohydrate oxidation compared to during metabolically-matched, steady-state exercise at SL. Methods: Using a randomized, crossover design, native lowlanders (n = 8 males, mean ± SD, age: 23 ± 2 yr, body mass: 87 ± 10 kg, and VO2peak: SL 4.3 ± 0.2 L/min and HA 2.9 ± 0.2 L/min) consumed 145 g (1.8 g/min) of glucose while performing 80-min of metabolically-matched (SL: 1.66 ± 0.14 V̇O2 L/min 329 ± 28 kcal, HA: 1.59 ± 0.10 V̇O2 L/min, 320 ± 19 kcal) treadmill exercise in SL (757 mmHg) and HA (460 mmHg) conditions after a 5-h exposure. Substrate oxidation rates (g/min) and glucose turnover (mg/kg/min) during exercise were determined using indirect calorimetry and dual tracer technique (13C-glucose oral ingestion and [6,6-2H2]-glucose primed, continuous infusion). Results: Total carbohydrate oxidation was higher (P < .05) at HA (2.15 ± 0.32) compared to SL (1.39 ± 0.14). Exogenous glucose oxidation rate was lower (P < .05) at HA (0.35 ± 0.07) than SL (0.44 ± 0.05). Muscle glycogen oxidation was higher at HA (1.67 ± 0.26) compared to SL (0.83 ± 0.13). Total glucose Ra was lower (P < .05) at HA (12.3 ± 1.5) compared to SL (13.8 ± 2.0). Exogenous glucose Ra was lower (P < .05) at HA (8.9 ± 1.3) compared to SL (10.9 ± 2.2). Glucose Rd was lower (P < .05) at HA (12.7 ± 1.7) compared to SL (14.3 ± 2.0). MCR was lower (P < .05) at HA (9.0 ± 1.8) compared to SL (12.1 ± 2.3). Circulating glucose and insulin concentrations were higher in response carbohydrate intake during exercise at HA compared to SL. Conclusion: Novel results from this investigation suggest that reductions in exogenous carbohydrate oxidation at HA may be multifactorial; however, the apparent insensitivity of peripheral tissue to glucose uptake may be a primary determinate.
Article
Assessment of risk of bias is regarded as an essential component of a systematic review on the effects of an intervention. The most commonly used tool for randomised trials is the Cochrane risk-of-bias tool. We updated the tool to respond to developments in understanding how bias arises in randomised trials, and to address user feedback on and limitations of the original tool.
Article
BACKGROUND: Initiating aerobic exercise with low muscle glycogen content promotes greater fat and less endogenous carbohydrate oxidation during exercise. However, the extent exogenous carbohydrate oxidation increases when exercise is initiated with low muscle glycogen is unclear. PURPOSE: Determine the effects of muscle glycogen content at the onset of exercise on whole-body and muscle substrate metabolism. METHODS: Using a randomized, crossover design, 12 men (mean ± SD, age: 21 ± 4 y; body mass: 83 ± 11 kg; VO2peak: 44 ± 3 mL/kg/min) completed 2 cycle ergometry glycogen depletion trials separated by 7-d, followed by a 24-h refeeding to elicit low (LOW; 1.5 g/kg carbohydrate, 3.0 g/kg fat) or adequate (AD; 6.0 g/kg carbohydrate, 1.0 g/kg fat) glycogen stores. Participants then performed 80-min of steady-state cycle ergometry (64 ± 3% VO2peak) while consuming a carbohydrate drink (95 g glucose +51 g fructose; 1.8 g/min). Substrate oxidation (g/min) was determined by indirect calorimetry and 13C. Muscle glycogen (mmol/kg dry weight), pyruvate dehydrogenase activity, and gene expression were assessed in muscle. RESULTS: Initiating steady-state exercise with LOW (217 ± 103) or AD (396 ± 70; P < 0.05) muscle glycogen did not alter exogenous carbohydrate oxidation (LOW: 0.84 ± 0.14, AD: 0.87 ± 0.16; P > 0.05) during exercise. Endogenous carbohydrate oxidation was lower and fat oxidation was higher in LOW (0.75 ± 0.29 and 0.55 ± 0.10) than AD (1.17 ± 0.29 and 0.38 ± 0.13; all P < 0.05). Before and after exercise PDH activity was lower (P < 0.05) and transcriptional regulation of fat metabolism (FAT, FABP, CPT1a, HADHA) was higher (P < 0.05) in LOW than AD. CONCLUSION: Initiating exercise with low muscle glycogen does not impair exogenous carbohydrate oxidative capacity, rather, to compensate for lower endogenous carbohydrate oxidation acute adaptations lead to increased whole-body and skeletal muscle fat oxidation.
Article
We examined whether carbohydrate-protein ingestion influences muscle glycogen metabolism during short-term recovery from exhaustive treadmill running and subsequent exercise. Six endurance-trained individuals underwent two trials in a randomised double-blind design, each involving an initial run-to-exhaustion at 70% VO2max (Run-1) followed by 4-h recovery (REC) and subsequent run-to-exhaustion at 70% VO2max (Run-2). Carbohydrate-protein (CHO-P; 0.8 g carbohydrate·kg body mass [BM-1]·h-1 plus 0.4 g protein·kg BM-1·h-1) or isocaloric carbohydrate (CHO; 1.2 g carbohydrate·kg BM-1·h-1) beverages were ingested at 30-min intervals during recovery. Muscle biopsies were taken upon cessation of Run-1, post-recovery and fatigue in Run-2. Time-to-exhaustion in Run-1 was similar with CHO and CHO-P (81±17 and 84±19 min, respectively). Muscle glycogen concentrations were similar between treatments after Run-1 (99±3 mmol·kg dry mass [dm-1]). During REC, muscle glycogen concentrations increased to 252±45 mmol·kg dm-1 in CHO and 266±30 mmol·kg dm-1 in CHO-P (p= 0.44). Muscle glycogen degradation during Run-2 was similar between trials (3.3±1.4 versus 3.5±1.9 mmol·kg dm-1·min-1 in CHO and CHO-P, respectively) and no differences were observed at the respective points of exhaustion (93±21 versus 100±11 mmol·kg dm-1·min-1; CHO and CHO-P, respectively). Similarly, time-to-exhaustion was not different between treatments in Run-2 (51±13 and 49±15 min in CHO and CHO-P, respectively). Carbohydrate-protein ingestion equally accelerates muscle glycogen resynthesis during short-term recovery from exhaustive running as when 1.2 g carbohydrate·kg BM-1·h-1 are ingested. The addition of protein did not alter muscle glycogen utilisation or time to fatigue during repeated exhaustive running.