Multiple Transportable Carbohydrates During Exercise: Current Limitations and Directions for Future Research.

BRIEF REVIEW

MULTIPLE TRANSPORTABLE CARBOHYDRATES DURING EXERCISE: CURRENT LIMITATIONS AND DIRECTIONS FOR FUTURE RESEARCH PATRICK B. WILSON Athletics Department, Nebraska Athletic Performance Laboratory, University of Nebraska–Lincoln, Lincoln, Nebraska ABSTRACT Wilson, PB. Multiple transportable carbohydrates during exercise: Current limitations and directions for future research. J Strength Cond Res 29(7): 2056–2070, 2015—The concept of multiple transportable carbohydrates (MTC) refers to a combination of saccharides that rely on distinct transporters for intestinal absorption. Ingestion of MTC during prolonged exercise has been purported to increase carbohydrate absorption efficiency, increase exogenous carbohydrate oxidation, reduce gastrointestinal (GI) distress, and improve athletic performance when carbohydrate intake is high (.50–60 g$h21). Although reviews of MTC research have been published previously, a comprehensive literature evaluation underscoring methodological limitations has not been conducted to guide future work. Accordingly, this review outlined the plausible mechanisms of MTC and subsequently evaluated MTC research based on several factors, including participant characteristics, exercise modality, exercise task, treatment formulation, treatment blinding, and pre-exercise nutrition status. A total of 27 articles examining MTC during exercise were identified and reviewed. Overall, ingestion of MTC led to increased exogenous carbohydrate oxidation, reduced GI distress, and improved performance during cycling lasting $2.5 hours, particularly when carbohydrate was ingested at $1.2 g$min21. Despite the apparent benefits, several limitations in the literature were apparent, including that only 3 studies used running, only 2 studies were conducted in the field, most participants were fasted, and women and adolescents were underrepresented. In addition, the majority of the studies fed carbohydrate at $1.2 g$min21, which may have inflated levels of GI distress and exaggerated performance decrements with singlesaccharide feedings. Based on these limitations, future MTC investigations should consider focusing on running, examining team-based sports, including women and adolescents,

conducting experiments under field conditions, examining the modifying effects of pre-exercise nutrition, and using modest feeding protocols (1.0–1.2 g$min21).

KEY WORDS endurance, fructose, nutrition INTRODUCTION

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uidelines from the American College of Sports Medicine and American Dietetic Association recommend that 30–60 g$h21 of carbohydrate be consumed during exercise lasting longer than 1 hour (51). Emerging evidence from the past 2 decades, however, demonstrates that higher rates of exogenous carbohydrate can be tolerated if the carbohydrate source is composed of multiple saccharides (e.g., mix of glucose and fructose (29)). Although the first of these studies focused on exogenous carbohydrate oxidation (1,64), subsequent work demonstrated improvements in endurance performance (11,29). Furthermore, several studies have shown that the risk of gastrointestinal (GI) distress is minimized when multiple saccharides are consumed (31,39,40,53,62). Research regarding the benefits of ingesting multiple saccharides during exercise— referred to as multiple transportable carbohydrates (MTC)— has been an exciting advancement in the field of sport nutrition, and these findings have been used by food manufacturers to market products as containing a superior blend of carbohydrate for performance and GI function (17,47). Despite several reviews covering the topic (9,28,29), a comprehensive literature evaluation underscoring methodological limitations has not been conducted to guide future MTC research. Therefore, the purpose of this review was to comprehensively evaluate MTC research, with a focus on methodological limitations to provide direction for future investigations.

METHODS Search Strategy

Address correspondence to Patrick B. Wilson, [email protected]. 29(7)/2056–2070 Journal of Strength and Conditioning Research Ó 2015 National Strength and Conditioning Association

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Studies were evaluated in terms of general design, participant characteristics, exercise modality, exercise/performance task, treatment formulation, treatment blinding, and preexercise nutrition status. Articles were identified based on the author’s knowledge of the literature, through previously

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Journal of Strength and Conditioning Research

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.

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Journal of Strength and Conditioning Research published reviews on the topic (9,28,29), and through database searches (PubMed and SPORTDiscus). Database searches were conducted using the following terminology: multiple transportable carbohydrate exercise, fructose glucose exercise, and sucrose glucose exercise. Only investigations that used a randomized experimental design during exercise at least 50% V_ O2peak were included. Studies with exercise durations lasting 1 hour or less were excluded because it is unlikely that carbohydrate ingestion is of benefit for shorter durations (51). Studies that compared 2 monosaccharide treatments (glucose vs. fructose) were not included; however, studies that compared a monosaccharide with sucrose were included because sucrose is composed of fructose and glucose and appears to be metabolized similarly as free glucose-fructose mixtures (66). Studies that fed a relatively low rate of carbohydrate (,45 g$h21) were excluded; as outlined by previous reviews, any benefits of MTC are unlikely to occur at lower carbohydrate intakes (28,29). Finally, only studies that matched for total carbohydrate delivery and electrolyte content were included. Thus, studies exclusively comparing MTC with a single saccharide, but with different total carbohydrate feeding rates, were excluded. As several excellent reviews have discussed previously in detail the mechanisms of MTC, the current review presents only a brief overview of plausible MTC mechanisms. Readers interested in a more comprehensive review of mechanisms are directed to the following references (28,29).

MULTIPLE TRANSPORTABLE CARBOHYDRATES: MECHANISMS OF BENEFIT Many of the proposed benefits of MTC stem from the metabolic and GI system effects of dietary fructose. Under resting conditions, concentrated fructose solutions (10–15%) empty faster from the stomach than isocaloric glucose solutions (18,58), which may be explained by the inhibitory feedback effects of glucose on afferent nerves in the small intestine (69). Once emptied from the stomach, glucose and fructose rely on distinct intestinal transporters for absorption into enterocytes. The major intestinal transporters for glucose and fructose are the sodium-dependent glucose cotransporter 1 (SGLT1) and glucose transporter-5 (GLUT5), although other transport systems are likely involved (67). Sodium-dependent glucose cotransporter 1 relies on secondary active transport to absorb glucose up a concentration gradient, whereas GLUT5 uses facilitated diffusion for the absorption of fructose into enterocytes. It has been theorized that SGLT1 becomes saturated when glucose is fed at a high rate (.50–60 g$h21), and therefore, supplying a mix of glucose and fructose would theoretically increase carbohydrate absorption and reduce GI distress when carbohydrate intake is high. Indeed, indirect evidence for this hypothesis comes from studies showing that increasing the dose of ingested glucose does not result in an absolute linear increase in exogenous glucose oxidation (28,29,57). Direct evidence for this hypothesis, however, is somewhat limited (28), although

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research using multiple-lumen sampling techniques provides confirmation that intestinal absorption could be a limiting factor for exogenous glucose oxidation (13,33). Fructose, in comparison with glucose, seems to have a lower capacity for absorption when ingested alone (16), resulting in 20–30% lower oxidation rates (22) and malabsorption (49). Fructose malabsorption, however, is minimized if it is co-ingested with glucose, as glucose stimulates fructose intestinal uptake (61). After being absorbed, the majority of fructose is metabolized by the liver, although the intestines may convert a small portion to lactate and glucose (61). Relative to glucose, fructose metabolism is less tightly regulated because its major point of entry into the glycolysis pathway bypasses the phosphofructokinase reaction. Importantly, phosphofructokinase activity is inhibited by adenosine triphosphate (ATP) and citrate, and a large influx of glucose into the liver can inhibit phosphofructokinase by altering the energy status of the cell (61). Fructose, however, enters the glycolytic pathway predominantly by phosphorylation to fructose-1-phosphate, which occurs downstream of phosphofructokinase. The entry of fructose carbons into glycolysis results in increased activity of pyruvate dehydrogenase (42), and as a result, an increase in blood lactate concentrations (23,24). Lactate produced from fructose ingestion during exercise is hypothesized to serve as substrate for oxidative energy production, by cell-to-cell and intracellular pathways (7,19). A review of tracer studies— during both rest and exercise—estimated that 25–30% of fructose is converted to lactate within a few hours of ingestion (60), and lactate oxidation may account for approximately half of exogenous fructose oxidation (34). The conversion of fructose to glucose by gluconeogenesis also increases in response to fructose feeding, providing an additional pathway for fructose carbon oxidation. The same review of tracer studies estimated that anywhere between 29 and 54% of fructose is converted to glucose within 2–6 hours of ingestion, depending on the dosage and metabolic health of an individual (60). Although these metabolic effects of fructose may be advantageous when energy demand is high (e.g., during exercise), they may also contribute to unfavorable effects in sedentary populations, such as dyslipidemia, fatty liver, and insulin resistance (61). Another potential advantage of glucose-fructose coingestion is enhanced fluid delivery during exercise. An increase in carbohydrate absorption could, in theory, increase water absorption by creating a favorable osmotic gradient across the epithelial cell barrier (38), as well as by increasing water cotransport by SGLT1 coupling (68). Consequently, increased absorption of carbohydrate molecules with MTC ingestion would be advantageous in terms of fluid delivery to the circulation. In support of this hypothesis, several studies have shown that markers of fluid delivery are improved with glucose-fructose co-ingestion compared with an equivalent concentration of glucose (30,50). Jeukendrup and Moseley (30) used several methods to compare fluid dynamics with the ingestion of a glucose-only solution or a 2:1 glucose-fructose solution VOLUME 29 | NUMBER 7 | JULY 2015 |

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Multiple Transportable Carbohydrates (1.5 g$min21). Sampling of stomach contents with a nasogastric tube was used to estimate gastric emptying, and an ingested deuterium tracer was used to estimate fluid delivery. After 45 minutes of exercise, a greater amount of the glucose-fructose solution had emptied from the stomach, and 5 minutes after tracer ingestion, plasma deuterium enrichment was greater with the glucose-fructose solution, suggesting more rapid fluid delivery (30). Additionally, Lambert et al. (33) used a multiple-lumen sampling technique to show that overall fluid delivery was higher with a glucose-fructose mixture, although this study was not performed during exercise. In terms of benefits to an athlete, improvements in gastric emptying and fluid delivery could help maintain plasma volume and reduce heart rate, especially in hot and humid environmental conditions. However, these benefits of MTC on cardiac physiology during exercise are predominantly speculative in nature. Finally, the effects of fructose on the central nervous system represent a possible, but largely underexplored, mechanism. A recent blinded study using functional magnetic resonance imaging found that glucose and fructose activate different brain regions and may have differential effects on reward and motivational processing (41), although it is unknown whether sweetness differences or other carbohydrate-specific oral receptors explain these findings. Both sweetness and carbohydrate structure are proposed to influence brain activity. Sweet substances cause cells on the tongue (G-protein–coupled receptor proteins T1R2 and T1R3) to release neurotransmitters that interact with primary afferent nerve fibers and the brainstem (5). Notably, fructose is sweeter than glucose (37).

Although data from humans are absent, experiments in rodents provide tentative evidence that carbohydrate structure may influence receptors in the mouth separately from sweetness. Rats preferred maltodextrin over sweeter saccharides such as sucrose, glucose, and fructose at low concentrations, and only at high concentrations did they prefer sucrose (56). In addition, experiments with knockout mice lacking either the T1R2 or T1R3 protein demonstrated reductions in the preference for sucrose (70) and artificial sweeteners (12). Much more research is clearly needed, however, to clarify whether fructose-specific and glucose-specific oral receptors are present in humans and whether they differentially activate brain regions that influence neuromuscular control and exercise performance.

EVALUATION

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CURRENT RESEARCH

Search Results

The process of article identification and exclusion is presented in Figure 1. A total of 560 articles were identified through the database searches. After excluding articles that failed to meet inclusion criteria and duplicate articles, a total of 26 articles remained. In addition, 1 recently published article was included based on the knowledge of the author, increasing the total number of included articles to 27 (Table 1). Benefits of Multiple Transportable Carbohydrates

Compared with single saccharides, ingesting a mix of glucose, fructose, and/or sucrose increased exogenous carbohydrate oxidation among the majority of studies feeding carbohydrate above 1.0 g$min21 (23–27,65). However, 1 study that fed

Figure 1. An overview of article identification and exclusion.

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TABLE 1. Review of studies examining multiple transportable carbohydrates during exercise (in chronological order).* Article

Participants

Maughan et al. (36)

6 untrained males

Design

Blinding

Not reported Randomized crossover of TTE cycling at 70% V_ O2peak

Wagenmakers et al. (64)

Not reported 6 male cyclists Randomized crossover of 120-min cycling at 65% peak power 6 healthy Randomized Not reported young men crossover of 120-min cycling at 61% V_ O2peak

Adopo et al. (1)

Fasted

100 ml of 35% solutions at exercise onset and every 10 min thereafter

CHO source CON: water, GLU: 3.8 g$min21 glu, FRU: 3.8 g$min21 fru, MTC: 2.2, 1.6 g$min21 glu-fru

Significant findings TTE was not different for GLU vs. MTC (79.0 vs. 79.5 min) but was longer than FRU (65.6 min)

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VOLUME 29 | NUMBER 7 | JULY 2015 |

None of the solutions were well tolerated Change in plasma 10 h fast 3.15 L total (1.05 CON: artificially volume trended toward L$h21) of 5% sweetened water; being lower with MTC solutions GLU1: 0.88 than GLU1 (22.6 vs. g$min21 glu; GLU2: 28.1%) 0.88 g$min21 md; MTC: 0.56, 0.32 g$min21 md-fru GLU1 resulted in greater postexercise gastric residual volume than CON, but GLU2 and MTC did not differ from CON Breakfast: 1 1.72 L total (860 CON: water; GLU: Total EXO of 76 and g$kg21 1.85 g$kg21 md; ml$h21) of 8% 81 g for GLU and MTC (not significantly solutions MTC: 1.85 g$kg21 bread and 5 different) ml$kg21 of suc CHO drink Dinner: CHO 500 ml bolus of CON: water; GLU1: MTC EXO was ;30% higher than GLU2 50 g glu; GLU2: 10–20% 110 g, 100 g glu; FRU1: solutions 5 min protein 70 g, 50 g fru; FRU2: after start of fat 40 g; 100 g fru; MTC: 50, exercise breakfast: 50 g glu-fru CHO 50 g, protein 15 g, fat 15 g (continued on next page)

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8 male cyclists Randomized Double-blind; crossover of success not 180-min cycling reported at 60% V_ O2peak in heat (338 C)

Fluid volume and concentration†


Ryan et al. (55)

Pre-exercise nutrition


the


12 nonathlete boys (aged 11–14 y)

Jentjens et al. (23) 8 trained male cyclists/ triathletes

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Participant Randomized single-blind; crossover of 90success not min cycling at reported 55% V_ O2peak followed by TTE at 90% peak power

Randomized crossover of 150-min of cycling at 62% V_ O2peak

Not reported

Randomized Not reported crossover of 120-min cycling at 63% V_ O2peak

1.12 L total (750 CON: artificially Breakfast: MTC EXO was ;14% ml$h21) of 6% white bread, sweetened water; less at 90 min than peanut GLU: 1.5 g$kg21 GLU solutions during butter, and the 90-min glu; MTC: 0.75, orange juice protocol 0.75 g$kg21 glu-fru

10–12 h fast

10–12 h fast



10–12 h fast



10–12 h fast

Wallis et al. (65)


10–12 h fast

8 trained male cyclists/ triathletes

1.95 L total (780 CON: plain water; GLU: 2.4 g$min21 ml$h21) of 18.5% glu; MTC: 1.2, 0.6, solutions 0.6 g$min21 glu-frusuc

1.65 L total (825 CON: plain water; GLU1: 1.2 g$min21 ml$h21) of 8.7 and 13.1% glu; GLU2: 1.8 solutions g$min21 glu; MTC: 1.2, 0.6 g$min21 glu-fru

TTE for CON was less than MTC but not different from GLU Peak MTC EXO was 44% higher than GLU

More subjects had severe GI discomfort with GLU Peak MTC EXO was 55% higher than GLU1 and GLU2

More subjects had severe GI discomfort with GLU2 than GLU1 and MTC 1.95 L total (780 CON: plain water; Peak MTC EXO was GLU1: 1.8 g$min21 ml$h21) of 18% higher than GLU1 and GLU2 13.8% glu; GLU2: 1.2, 0.6 solutions g$min21 glu-md; MTC: 1.2, 0.6 g$min21 glu-suc EXO for SUC and MTC1 1.65 L total (825 CON: plain water; GLU: 1.2 g$min21 were 20–30% higher ml$h21) of 8.7 than GLU and 17.5% glu; SUC: 1.2 solutions g$min21 suc; MTC1: 0.6, 0.6 g$min21 glu-suc; MTC2: 1.2, 1.2 g$min21 glu-suc CON: plain water; 2.4 L total (960 Peak MTC EXO was GLU: 1.8 g$min21 ml$h21) of ;40% higher than GLU for last 30 min 11.3% md; MTC: 1.2, 0.6 solutions g$min21 md-fru


Multiple Transportable Carbohydrates

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Riddell et al. (48)


Jeukendrup et al. (31)


Currell and 8 trained male Jeukendrup (11) cyclists

Randomized crossover of 120-min cycling at 50% peak power conducted in heat (328 C)

Not reported

Randomized Participant crossover of single-blind; 300-min cycling success not at 58% V_ O2peak reported

Not reported

Stannard et al. (59)

2.25 L total (750 CON: water; GLU: ml$h21) of 1.8 g$min21 glu; 14.4% MTC: 1.2, 0.6 solutions g$min21 glu-fru

10–12 h fast

1.95 L total (780 CON: plain water; ml$h21) of 6% GLU: 0.8 g$min21 glu; MTC: 0.5, 0.3 solutions g$min21 glu-fru Consumed CHO as gels with GLU: 1.4 g$min21 their “usual” water intake of glu; MTC: 0.9, 0.5 prerace meal ;400 ml g$min21 glu-fru

Overnight fast

0.9 L$h21 of 8% solutions

Pedal cadence was maintained only with MTC GLU resulted in greater fullness over the last hour than MTC CHO oxidation not different

MTC resulted in 8% quicker time to completion than GLU EXO not different between GLU and MTC No performance differences

Several GI symptoms higher with MTC than GLU GAL resulted in slower GAL: 1.0 g$min21 TT performance gal; MTC1: 0.5, 0.5 (;15%) than MTC1 g$min21 gal-glu; and MTC2 MTC2: 0.8, 0.2 g$min21 glu-fru (continued on next page)


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Double-blind; 9 male cyclists Randomized success not crossover of reported 120-min cycling at 65% V_ O2peak followed by a ;30 min TT

CON: water; GLU: 1.5 g$min21 glu; MTC: 1.0, 0.5 g$min21 glu-fru

RPE at the end was higher with GLU than MTC Mean MTC EXO was ;13% higher than GLU

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Randomized Participant crossover of single-blind; 150-min cycling success not at 65% V_ O2peak reported Double-blind; Pfeiffer et al. (44) 48 runners (34 Randomized success not males, 14 crossover of 16reported females) km TT outdoor run

Not reported

4.4 L total (880 ml$h21) of ;10% solutions

MTC EXO was 36% higher than GLU for last hour

the

Hulston et al. (21) 7 trained male cyclists

Overnight fast

2.0 L total (1,000 CON: plain water; ml$h21) of 9% GLU: 1.5 g$min21 glu; MTC: 1.0, 0.5 solutions g$min21 glu-fru


Randomized crossover of 120-min cycling at 55% peak power followed by ;1 h TT

10–12 h fast

the


8 male subjects

Lecoultre et al. (34)

7 trained male cyclists

Triplett et al. (63)

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O’Brien and Rowlands (39)

Clarke et al. (10)

Randomized Participant crossover of single-blind; 120-min cycling success not at 61% V_ O2peak reported

Randomized Participant crossover of single-blind; 120-min cycling success not at 60% V_ O2peak reported Double-blind; 9 male cyclists Randomized success not crossover 100reported km TT on a cycle ergometer 10 trained male Randomized crossover of cyclists/ 150-min cycling triathletes at 50% peak power followed by an incremental test to exhaustion

11 male university soccer players

Double-blind; success nonformally reported

Randomized Double-blind; crossover of 90success not min soccerreported specific protocol followed by a run at 12.8 km$h21 and 20% gradient

10–11 h fast

2.1 L total (1.05 CON: water; GLU: L$h21) of 8.6% 1.5 g$min21 glu; solutions MTC: 1.0, 0.5 g$min21 glu-fru

Overnight fast

2.0 L total (1.0 L$h21) of 12% solutions

GLU: 2.0 g$min21 glu; MTC: 1.2, 0.8 g$min21 glu-fru

10–12 h fast

3.8 L total (1.05 L$h21) of 14.4% solutions

GLU: 2.4 g$min21 glu; MTC: 1.2, 1.2 g$min21 glu-fru

Overnight fast

2.8 L total (1.12 L$h21) of 13.5% solutions

CON: artificially sweetened water; MTC1: 1.2, 0.6 g$min21 md-fru; MTC2: 1.0, 0.8 g$min21 md-fru; MTC3: 0.8, 1.0 g$min21 md-fru

Average daily 1.37 L total (913 CON: sweetened ml$h21) of intake of 375 water; GLU: 1.0 g CHO, but g$min21 glu; MTC: 6.6% solutions no report of over the soccer 0.66, 0.33 g$min21 meal before protocol glu-fru protocol

7 participants felt very full with GLU Higher peak power for MTC2 and MTC3 than MTC1 and CON

Stomach fullness, cramping, and nausea were lowest with MTC2 CHO oxidation not different

Trend for longer TTE with MTC vs. GLU



2062 Jeukendrup and Moseley (30)

TT performance was not different between MTC1 and MTC2 MTC resulted in faster gastric emptying, lower leg RPE, and lower heart rate than GLU MTC resulted in higher total CHO (7%) and lactate oxidation (30%) than GLU TT 7.5% faster with MTC vs. GLU

Rowlands et al. (53)

Double-blind; Randomized Field: 10 success not crossovers; field: trained reported ;140-min cyclists (7 mountain bike males and 3 race; laboratory: females); 94-min setLaboratory: workload 16 trained intervals male cyclists followed by 10 maximal sprints

O’Brien et al. (40) 12 trained male Randomized crossover of cyclists/ 120-min cycling triathletes at 57% peak power followed by 10 sprints

8 trained male cyclists

Randomized crossover of 150-min cycling at 50% peak power followed by 60-km TT

Double-blind; success not reported

12 h fast

;500 calorie meal 2 h before

1.08 L$h21 of 9% GLU: 1.7 g$min21 solutions md; MTC1: 0.84, 0.52, 0.34 g$min21 md-fru-protein; MTC2: 1.1, 0.6 g$min21 md-fru

TT 2 and 5% faster with MTC2 than MTC1 and GLU Most GI symptoms were more prevalent with GLU TT was 3% faster for MTC than GLU2

(continued on next page)

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2.25 L total (750 CON: artificially ml$h21) of 8– sweetened water; 12% solutions GLU1: 1.03 g$min21 glu; GLU2: 1.55 g$min21 glu; MTC: 1.03, 0.52 g$min21 glu-fru

Mean sprint power was highest with MTC2 Peak MTC2 EXO was 40–45% higher than GLU and MTC1

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1.8 L total (900 CON: artificiallyml$h21) of sweetened water; MTC1: 0.67, 0.33, 11.3% 0.5 g$min21 mdsolutions during the 120-min glu-fru; MTC2: period 0.67, 0.16, 0.67 g$min21 md-glu-fru; MTC3: 0.67, 0.83 g$min21 md-fru

the


Baur et al. (3)


Double-blind; Overnight fast differences in sweetness

MTC reduced abdominal cramps in the field and nausea in the laboratory MTC2 EXO was 18 and 5% higher than MTC1 and MTC3


Tarpey et al. (62)

Field: CHO of Field: 1.62 L total Field: GLU: 0.9, 0.45 Field and lab 6.5 g$kg21; g$min21 md-glu; of 11.5% performance improved solutions; by 1.4–1.8% with laboratory: MTC: 0.9, 0.45 laboratory: 2.86 MTC vs. GLU 250 ml water g$min21 md-fru; L total of 9.0% + 14 g laboratory: GLU: solutions cereal bar 1.0, 0.5 g$min21 10 minutes md-glu; MTC: 1.0, before 0.5 g$min21 md-fru

the


Lee et al. (35)



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Double-blind; 15 recreational Randomized success not crossover of halfrunners (12 reported marathon on males and 3 a treadmill females)

12 h fast

1.08 L$h21 of 10% solutions

CON: artificially sweetened water; GLU: 1.7 g$min21 md; MTC: 1.1, 0.6 g$min21 md-fru

Breakfast: 2 1.56 L total of 6% GLU1: 1.0 g$min21 21 g$kg of solution or glu (beverage); CHO gels with CHO, 30 g GLU2: 1.0 g$min21 ad libitum fluid protein, and glu (gel); MTC: intake (404– 10 g fat (2.5 0.65, 0.35 g$min21 473 ml total) h before) glu-fru (gel)

GI symptoms were most prevalent with GLU MTC resulted in greater fluid delivery than GLU MTC TT performance was 7% faster than GLU No significant performance differences, but effect sizes for MTC vs. GLU1 and GLU2 were modest (2.7 and 3% slower for MTC) No differences for HR, RPE, and GI discomfort Plasma glucose was lower with MTC than GLU1 and GLU2

*CHO = carbohydrate; CON = control; EXO = exogenous carbohydrate oxidation; fru = fructose; gal = galactose; glu = glucose; HR = heart rate; md = maltodextrin; MTC = multiple transportable carbohydrates; RPE = rating of perceived exertion; suc = sucrose; TT = time trial; TTE = time-to-exhaustion. †Some volumes and concentrations had to be estimated, as some studies did not provide an exact total volume.



2064 Roberts et al. (50) 14 male club cyclists

TT performance differences were unclear between MTC and GLU1 MTC EXO was ;36% higher at the end of exercise than GLU

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Journal of Strength and Conditioning Research ;1.2 g$min21 of carbohydrate as sucrose or maltodextrin did not find any statistically significant differences in exogenous carbohydrate oxidation (64). Studies that fed carbohydrate at ,1.0 g$min21 have been equivocal, finding higher (1), equivalent (21), or lower rates (48) of exogenous carbohydrate oxidation with MTC. Although the study by Adopo et al. (1) showed that 0.8 g$min21 of glucose-fructose led to higher exogenous carbohydrate oxidation relative to glucose only, it must be noted that a large concentrated bolus at the start of exercise was used instead of smaller boluses interspersed over the entire protocol. As a result, gastric emptying in the glucose-only condition could have been substantially reduced at the start of exercise, which could have contributed to the lower exogenous carbohydrate oxidation. In terms of performance, MTC improved outcomes (e.g., completion time, exercise capacity, and power output) in 8 studies (3,11,39,40,53,59,62,63). The largest effect on performance was from the study by Stannard et al. (59), in which 1.0 g$min21 of galactose led to ;15% slower time trial (TT) completion compared with glucose-galactose and glucosefructose mixtures. Three additional studies found performance improvements as large as 7–8% for TT completion with glucose-fructose feedings relative to glucose-only feedings (11,50,63). Multiple transportable carbohydrates reduced GI complaints in several studies, including stomach fullness (31,39,50), nausea (40,50,62), abdominal cramps (40,53,62), and the urge to defecate (50). Two studies support the notion that fluid delivery is more rapid with glucose-fructose mixtures (30,50), whereas another suggests that decreases in plasma volume may be minimized (55). Several other studies provide evidence that ratings of perceived exertion are lower with glucose-fructose mixtures (26,30,50). Despite these encouraging findings, various study design factors make interpretation and application of the results somewhat limited. These study design factors are subsequently outlined. Study and Participant Characteristics

All 27 studies used a crossover design to investigate the effects of MTC during exercise. Sample sizes have generally been small, with only 3 studies reporting samples of 15 or greater (35,44,53). Despite the often small sample sizes, statistical power analyses or sample size calculations were undertaken for only 9 studies (3,10,30,35,40,50,53,62,65). Of the 27 studies, 25 were conducted within a laboratory environment, whereas 2 were conducted under field conditions (44,53). One of the 2 studies conducted under field conditions found a performance benefit during mountain biking (53), whereas the other did not find a performance benefit during simulated outdoor 16-km running (44). Twenty-four of the studies exclusively included men; 3 studies included women (35,44,53) for a total representation of 20 of 294 (7%) participants. Most of the participants were described as trained cyclists or triathletes, and further details on training or competition history were infrequently

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provided. All the studies were conducted with adults, with the exception of the study by Riddell et al. (48), which examined the effects of MTC during 90 minutes of cycling in boys aged 11–14 years. Based on the available evidence, it is not entirely clear whether the ingestion of MTC is beneficial for women, for adolescent populations, and under ecologically valid field conditions. Exercise Modality

Twenty-four of the 27 investigations used cycling as the exercise modality, whereas 3 studies examined MTC during running-based activities (10,35,44). Pfeiffer et al. (44) examined the effects of glucose-only and glucose-fructose gels on performance during 16-km outdoor runs, with both conditions providing carbohydrate at 1.4 g$min21. Overall, run times were not significantly different between conditions (1:14:25 for glucose vs. 1:14:41 for glucose-fructose). Contrary to expectations, the glucose-fructose gels seemed to cause more reflux, abdominal cramps, and loose stools. Similarly, Lee et al. (35) examined the effects of glucose-only and glucose-fructose ingestion on treadmill half-marathon TT performance. Carbohydrate was supplied at roughly 1.0 g$min21 in 3 conditions, which consisted of a 6% glucoseonly beverage, a glucose-only gel, and a glucose-fructose gel. Overall, there were no significant perceptual or performance differences between the conditions, although relative effect sizes between the conditions were modest in size (glucosefructose gel resulted in 2.7 and 3.0% slower finishing times; 35). In terms of metabolic effects, the glucose-fructose gel resulted in significantly lower plasma glucose levels and a trend toward lower total carbohydrate oxidation (35). It should be noted that the studies by Pfeiffer et al. (44) and Lee et al. (35) both had participants consume fluid ad libitum during the gel trials, which resulted in slightly different fluid intakes between the conditions. The other running-based study had 11 men completing 90-minute soccer protocols while ingesting carbohydrate at 1.0 g$min21 from glucose or a 2:1 glucose-fructose mix (10). After the 90-minute protocol, participants ran to exhaustion on a treadmill at 12.8 km$h21 and a 20% grade. Time-toexhaustion (TTE) and postexercise muscle glycogen levels were not significantly different between trials, but outcomes were statistically underpowered (power of 0.18 and 0.36 for muscle glycogen and TTE, respectively), and there was a trend for longer TTE in the glucose-fructose trial (83 6 9.7 vs. 77 6 7.2 seconds; p # 0.06). The 6-second difference in performance between the conditions equates to a 7% improvement in endurance capacity, which could represent a practically meaningful difference for certain athletic events (2). The lack of research using running-based activities is somewhat unfortunate because GI distress is more common during running (43), and running is the most popular endurance sport in the United States, with approximately 500,000 individuals finishing a marathon in 2011 (54). Two of the studies that used running showed trends toward negative VOLUME 29 | NUMBER 7 | JULY 2015 |

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Multiple Transportable Carbohydrates effects of glucose-fructose ingestion on GI comfort (44), plasma glucose maintenance (35), and performance (35), whereas the other study demonstrated a trend toward a positive effect on performance (10). Given the inconsistencies and lack of research using running, more studies are needed to determine if MTC improve performance for a range of running distances and intensities. In addition, further research examining the effects of MTC during prolonged, intermittent-intensity, team-based sports (basketball, rugby, and soccer) seems warranted. Exercise and Performance Tasks

Most studies used a constant intensity submaximal protocol to assess the metabolic effects of MTC, and the submaximal protocols were often followed by a TT to assess performance. The intensity of submaximal protocols was based on a percentage of peak oxygen consumption or cycling power output, and in general, 50–60% of peak power or 55–70% of peak oxygen consumption was used. Exercise durations ranged from approximately 75 minutes (44) to 300 minutes (31). For investigations that measured performance, the type of test used varied from study to study. Four studies used a pure TT with no previous submaximal protocol, 2 of which found a performance benefit (53,63), whereas 2 others did not (35,44). The difference between these studies may be attributable, in part, to the exercise durations used, as Triplett et al. (63) and Rowlands et al. (53) used cycling protocols lasting between 140 and 210 minutes, whereas Pfeiffer et al. (44) and Lee et al. (35) used running tasks lasting less than 120 minutes. In general, studies that used an exercise task lasting less than 120 minutes found no benefit to performance (10,35,44), indicating there may be a threshold effect of duration. Carbohydrate and Fluid Delivery Rate

Carbohydrate dosages ranged from 0.8 to 3.8 g$min21 (1,36,48), and as discussed, several studies that provided carbohydrate at #1.0 g$min21 did not find significant metabolic or performance benefits with MTC (10,21,35). Thus, when carbohydrate is ingested at #1.0 g$min21, it does not seem to matter whether the source is exclusively glucose or a glucose-fructose mixture. Less clear, however, is whether improvements in performance with MTC are apparent at modest carbohydrate feeding rates (;1.0–1.2 g$min21). Notably, many of the studies used beverage volumes that were quite large and solutions that were highly concentrated, which was likely done because the investigators recognized that at lower rates of carbohydrate ingestion (#1.0 g$min21), performance differences were unlikely to emerge. As a consequence, relatively few investigations have examined the effects of MTC at intermediate carbohydrate feeding rates (;1.0–1.2 g$min21). Other authors have previously highlighted this limitation and have attempted to address it with more modest feeding protocols (3,53). Baur et al. (3) provide the strongest support that previous protocols may have been overly aggressive.

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Specifically, high and moderate rates of glucose ingestion (1.55 and 1.03 g$min21) were compared with a high rate of glucose-fructose ingestion (1.55 g$min21) during ;2.5 hours of cycling. Notably, glucose-fructose ingestion significantly improved performance by 3% relative to high, but not moderate, glucose ingestion. The authors speculated that the amount of glucose consumed in previous studies likely resulted in considerable GI distress that impaired performance (3). On the whole, the results suggest that feeding a high rate of carbohydrate ($1.5 g$min21) as MTC will lead to improvements in performance compared with equal dosages of glucose-only feedings, but compared with moderate glucose intakes (1.0–1.2 g$min21), the benefits may not be as readily apparent (Figure 2 for an illustration of this concept). Therefore, additional research is needed to compare the GI and performance effects of high glucose-fructose intakes with moderate glucose intakes (1.0–1.2 g$min21). Another limitation to the research is the lack of comparison with ad libitum intake. Indeed, none of the 27 studies compared an ad libitum carbohydrate strategy with structured feeding schedules, although 2 studies did rely on ad libitum water intake with structured carbohydrate gel intake (35,44). In nonsimulated events, athletes rarely consume fluid at $1,000 ml$h21, even while cycling (45,52). Eight studies (26,30,34,39,50,55,62,63) provided fluid at $1,000 ml$h21, which is important to consider because athletes naturally limit fluid intake to minimize GI distress. In addition, the carbohydrate concentration of experimental solutions was at least 10% in 16 studies (1,3,11,23–25,27,31,34,36,39,40,50,53,63,65). It is known that increasing beverage concentration above 10% significantly inhibits gastric emptying, even for beverages that contain fructose (58). Consequently, forcing participants to consume concentrated beverages above ad libitum levels may have created conditions that limit the applicability of the results. A prime example of this comes from the study by Triplett et al. (63), in which participants finished a 100-km cycling TT 7.5% faster when consuming a glucose-fructose beverage compared with a glucose-only beverage. The beverages were 14.4% carbohydrate solutions supplied at 1,000 ml$h21, which provided carbohydrate at 2.4 g$min21. At this high feeding rate, 2 of 9 participants experienced diarrhea and 1 experienced vomiting with the glucose-only beverage. Furthermore, 7 of the 9 participants reported feeling as if their stomach were not emptying during the glucoseonly trial (63). It is reasonable to speculate that these individuals would not have selected such a high rate of carbohydrate intake on their own, even with the glucose-fructose beverage. Overall, the available data do not allow for strong conclusions to be made regarding the effects of high glucosefructose ingestion relative to an ad libitum strategy. Treatment Form and Blinding

Many carbohydrate sport supplements are marketed and sold worldwide, including beverages, gels, semisolids, powders,

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of participant blinding, as these are consensus recommendations for the implementation of high-quality randomized trials (14). Furthermore, studies matching for sweetness between conditions are needed to delineate if, and to what extent, sweetness profile contributes to performance improvements with glucose-fructose ingestion. Pre-exercise Nutrition Status

Seven studies reported acute preprotocol diet or provided food for participants Figure 2. As an example of most studies to date, the dashed line demonstrates that GI distress is lower with (1,3,35,44,48,53,64), whereas 21 glucose-fructose compared with glucose only when carbohydrate is ingested at $1.5 g$min ; however, when the majority of studies were comparing high glucose-fructose (1.5 g$min21) with moderate glucose-only (1.0–1.2 g$min21) ingestion, it is less clear which condition leads to more GI distress. As shown by the red ovals, GI distress may in fact be the same for conducted with participants moderate glucose-only (1.0–1.2 g$min21) and high glucose-fructose (1.5 g$min21) ingestion. Given the fasted. Fasting before exercise importance of GI distress in mediating performance outcomes, some of the previous literature may have results in a greater reliance on exaggerated the performance benefits associated with MTC. GI: gastrointestinal. fat oxidation, reduced muscle glycogen, and lower total carand others products. All but 2 of the studies used beverages to bohydrate oxidation (32). Consequently, the estimates of supply carbohydrate (35,44). Notably, the 2 studies that used exogenous carbohydrate oxidation should be interpreted a solid or semisolid form of carbohydrate (gels) failed to show somewhat cautiously, as differences between the conditions a benefit to performance with glucose-fructose ingestion, and may be exaggerated. In addition, performance effects for it seemed that the glucose-fructose gels caused more reflux, nutrition interventions may be larger under fasting condiabdominal cramps, and loose stools (44) and reduced plasma tions (4), so additional research should be considered to glucose (35). Other research has compared the effectiveness of determine if pre-exercise nutrition moderates the efficacy different forms of carbohydrate, and on the whole, liquid, of MTC. With that said, 2 studies do provide evidence that semisolid, and solid forms seem to be equally effective in glucose-fructose ingestion improves endurance cycling perterms of performance (8,46). An increasing number of conformance under fed conditions (3,53). sumers prefer “natural” alternatives that are minimally proPRACTICAL APPLICATIONS cessed and contain no artificial ingredients (15). Although the use of refined ingredients in previous MTC research has A multitude of studies provide evidence that the MTC helped control for confounding factors, it also reduces the ingestion—most commonly as a glucose-fructose mixture— generalizability of findings. Notably, endurance athletes freenhances exogenous carbohydrate oxidation, reduces GI disquently consume foods not specifically developed for sport, tress, and improves cycling performance at carbohydrate such as fruit, juice, sweet cakes, cookies, sandwiches, and intake $1.2 g$min21 As a result, a clear recommendation cereal (6,20). Consequently, future studies might consider can be given to male cyclists to consume MTC during conhow “natural” foods containing different saccharide profiles tinuous moderate-intensity (55–70% peak oxygen consumpaffect metabolism, performance, and GI distress. tion) cycling that lasts longer than 2–3 hours, especially if Many early MTC studies failed to report whether treatathletes are self-selecting to a high carbohydrate intake ments were participant blinded or investigator blinded, ($1.2 g$min21). When closely examining the literature, whereas most of the studies published since 2006 have however, it is less clear whether the use of MTC is relevant reported blinding status (Table 1). Although treatment blinding at moderate carbohydrate dosages (1.0–1.2 g$min21). Furhas increasingly been reported, many studies failed to provide thermore, the majority of studies used cycling, and none of details on the success of blinding or how the blinding was the 3 studies that used running demonstrated convincing performed. Specifically, only 1 study formally evaluated senbenefits with MTC. In addition, women have been undersory characteristics of treatments, with differences in sweetness represented up until this time, which is unfortunate because being reported (40). As a consequence, it is unknown whether female participation in endurance events has increased drasensory characteristics contributed significantly to the performatically over the last several decades (54). Likewise, only 1 mance benefits observed with MTC. Future studies should study examined the efficacy of MTC in children and adolesclearly outline blinding procedures and evaluate the success cents. Finally, most investigations had participants fast or did VOLUME 29 | NUMBER 7 | JULY 2015 |

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Multiple Transportable Carbohydrates not report pre-exercise nutrition intake, and only 1 study provided information on beverage sensory characteristics. Based on these limitations, it is recommended that future MTC research should focus on running, examining teambased sports, including women and adolescents, conducting experiments under field conditions, examining the modifying effects of pre-exercise nutrition, using modest feeding protocols, and evaluating sensory characteristics of treatments. In addition, other questions regarding MTC still remain to be answered, and although not meant to be a comprehensive list, several examples are outlined below: 1. Do GI disturbances decrease with repeated exposures to glucose-only feedings, thereby mitigating some of the proposed negative effects? 2. Do feeding frequency and bolus volume modify the GI and performance effects of MTC? 3. How does habitual diet (high vs. moderate and low carbohydrate) affect the response to MTC feedings? 4. What are the mechanisms responsible for improved psychological affect observed with MTC? 5. Do mixed glucose-fructose feedings, relative to glucoseonly, result in differential brain activation patterns during exercise? 6. To what extent do athletes from a variety of sports and competitions use foods containing MTC? 7. To what extent are athletes aware of the research and recommendations regarding MTC? 8. Given emerging evidence in sedentary populations, are there any health concerns for athletes frequently consuming fructose during exercise? The examination of these and other relevant questions will not only further our understanding of the physiological effects of MTC but will hopefully allow practitioners and athletes to apply the research in ways that influence athletic performance. Although past research has provided a solid foundation to build upon, future research needs to consider how the ingestion of MTC can be practically applied for a wider range of athletes and sports.

ACKNOWLEDGMENTS The author discloses no conflicts of interest. The entirety of this article was conceived and drafted by P. B. Wilson.

REFERENCES 1. Adopo, E, Pe´ronnet, F, Massicotte, D, Brisson, GR, and HillaireMarcel, C. Respective oxidation of exogenous glucose and fructose given in the same drink during exercise. J Appl Physiol 76: 1014– 1019, 1994. 2. Batterham, AM and Hopkins, WG. Making meaningful inferences about magnitudes. Int J Sports Physiol Perform 1: 50–57, 2006. 3. Baur, DA, Schroer, AB, Luden, ND, Womack, CJ, Smyth, SA, and Saunders, MJ. Glucose-fructose enhances performance versus isocaloric, but not moderate, glucose. Med Sci Sports Exerc 46: 1778–1786, 2014. 4. Beelen, M, Berghuis, J, Bonaparte, B, Ballak, SB, Jeukendrup, AE, and van Loon, LJ. Carbohydrate mouth rinsing in the fed state: Lack

2068

the

of enhancement of time-trial performance. Int J Sports Nutr Exerc Metab 19: 400–409, 2009. 5. Berthoud, HR. Neural systems controlling food intake and energy balance in the modern world. Curr Opin Clin Nutr Metab Care 6: 615–620, 2003. 6. Black, KE, Skidmore, PM, and Brown, RC. Energy intakes of ultraendurance cyclists during competition, an observational study. Int J Sports Nutr Exerc Metab 22: 19–23, 2012. 7. Brooks, GA. Lactate shuttles in nature. Biochem Soc Trans 30: 258– 264, 2002. 8. Campbell, C, Prince, D, Braun, M, Applegate, E, and Casazza, GA. Carbohydrate-supplement form and exercise performance. Int J Sports Nutr Exerc Metab 18: 179–190, 2008. 9. Cermak, NM and van Loon, LJ. The use of carbohydrates during exercise as an ergogenic aid. Sports Med 43: 1139–1155, 2013. 10. Clarke, ND, Campbell, IT, Drust, B, Evans, L, Reilly, T, and Maclaren, DP. The ingestion of combined carbohydrates does not alter metabolic responses or performance capacity during soccerspecific exercise in the heat compared to ingestion of a single carbohydrate. J Sports Sci 30: 699–708, 2012. 11. Currell, K and Jeukendrup, AE. Superior endurance performance with ingestion of multiple transportable carbohydrates. Med Sci Sports Exerc 40: 275–281, 2008. 12. Damak, S, Rong, M, Yasumatsu, K, Kokrashvili, Z, Varadarajan, V, Zou, S, Jiang, P, Ninomiya, Y, and Margolskee, RF. Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301: 850–853, 2003. 13. Duchman, SM, Ryan, AJ, Schedl, HP, Summers, RW, Bleiler, TL, and Gisolfi, CV. Upper limit for intestinal absorption of a dilute glucose solution in men at rest. Med Sci Sports Exerc 29: 482–488, 1997. 14. Fergusson, D, Glass, KC, Waring, D, and Shapiro, S. Turning a blind eye: The success of blinding reported in a random sample of randomised, placebo controlled trials. BMJ 328: 432, 2004. 15. Food Marketing Institute. Natural and Organic Foods, 2003. Available at: http://www.fda.gov/ohrms/dockets/dockets/06p0094/06p0094-cp00001-05-Tab-04-Food-Marketing-Institute-vol1.pdf. Accessed January 6, 2013. 16. Fujisawa, T, Mulligan, K, Wada, L, Schumacher, L, Riby, J, and Kretchmer, N. The effect of exercise on fructose absorption. Am J Clin Nutr 58: 75–79, 1993. 17. GU Pure Performance Energy. GU Energy gel. Available at: https:// guenergy.com/products/products-energy-gels/. Accessed October 10, 2013. 18. Guss, JL, Kissileff, HR, and Pi-Sunyer, FX. Effects of glucose and fructose solutions on food intake and gastric emptying in nonobese women. Am J Physiol 267: R1537–R1544, 1994. 19. Hashimoto, T and Brooks, GA. Mitochondrial lactate oxidation complex and an adaptive role for lactate production. Med Sci Sports Exerc 40: 486–494, 2008. 20. Havemann, L and Goedecke, JH. Nutritional practices of male cyclists before and during an ultraendurance event. Int J Sports Nutr Exerc Metab 18: 551–566, 2008. 21. Hulston, CJ, Wallis, GA, and Jeukendrup, AE. Exogenous CHO oxidation with glucose plus fructose intake during exercise. Med Sci Sports Exerc 41: 357–363, 2009. 22. Jandrain, BJ, Pallikarakis, N, Normand, S, Pirnay, F, Lacroix, M, Mosora, F, Pachiaudi, C, Gautier, JF, Scheen, AJ, Riou, JP, and Lefebvre, PJ. Fructose utilization during exercise in men: Rapid conversion of ingested fructose to circulating glucose. J Appl Physiol 74: 2146–2154, 1993. 23. Jentjens, RL, Achten, J, and Jeukendrup, AE. High oxidation rates from combined carbohydrates ingested during exercise. Med Sci Sports Exerc 36: 1551–1558, 2004.

TM



the

TM

Journal of Strength and Conditioning Research 24. Jentjens, RL, Moseley, L, Waring, RH, Harding, LK, and Jeukendrup, AE. Oxidation of combined ingestion of glucose and fructose during exercise. J Appl Physiol 96: 1277–1284, 2004. 25. Jentjens, RL, Shaw, C, Birtles, T, Waring, RH, Harding, LK, and Jeukendrup, AE. Oxidation of combined ingestion of glucose and sucrose during exercise. Metabolism 54: 610–618, 2005. 26. Jentjens, RL, Underwood, K, Achten, J, Currell, K, Mann, CH, and Jeukendrup, AE. Exogenous carbohydrate oxidation rates are elevated after combined ingestion of glucose and fructose during exercise in the heat. J Appl Physiol 100: 807–816, 2006. 27. Jentjens, RL, Venables, MC, and Jeukendrup, AE. Oxidation of exogenous glucose, sucrose, and maltose during prolonged cycling exercise. J Appl Physiol 96: 1285–1291, 2004. 28. Jeukendrup, AE. Carbohydrate intake during exercise and performance. Nutrition 20: 669–677, 2004.

| www.nsca.com

43. Peters, HP, van Schelven, FW, Verstappen, PA, de Boer, RW, Bol, E, Erich, WB, van der Togt, CR, and de Vries, WR. Gastrointestinal problems as a function of carbohydrate supplements and mode of exercise. Med Sci Sports Exerc 25: 1211–1224, 1993. 44. Pfeiffer, B, Cotterill, A, Grathwohl, D, Stellingwerff, T, and Jeukendrup, AE. The effect of carbohydrate gels on gastrointestinal tolerance during a 16-km run. Int J Sports Nutr Exerc Metab 19: 485– 503, 2009. 45. Pfeiffer, B, Stellingwerff, T, Hodgson, AB, Randell, R, Po¨ttgen, K, Res, P, and Jeukendrup, AE. Nutritional intake and gastrointestinal problems during competitive endurance events. Med Sci Sports Exerc 44: 344–345, 2012. 46. Pfeiffer, B, Stellingwerff, T, Zaltas, E, and Jeukendrup, AE. CHO oxidation from a CHO gel compared with a drink during exercise. Med Sci Sports Exerc 42: 2038–2045, 2010.

29. Jeukendrup, AE. Carbohydrate and exercise performance: The role of multiple transportable carbohydrates. Curr Opin Clin Nutr Metab Care 13: 452–457, 2010.

47. PowerBar. C2MAX performance Energy Video. Available at: http:// www.powerbar.com/nutrition-in-training/c2max-video. Accessed October 10, 2013.

30. Jeukendrup, AE and Moseley, L. Multiple transportable carbohydrates enhance gastric emptying and fluid delivery. Scand J Med Sci Sports 20: 112–121, 2010.

48. Riddell, MC, Bar-Or, O, Wilk, B, Parolin, ML, and Heigenhauser, GJ. Substrate utilization during exercise with glucose and glucose plus fructose ingestion in boys ages 10–14 yr. J Appl Physiol 90: 903–911, 2001.

31. Jeukendrup, AE, Moseley, L, Mainwaring, GI, Samuels, S, Perry, S, and Mann, CH. Exogenous carbohydrate oxidation during ultraendurance exercise. J Appl Physiol 100: 1134–1141, 2006. 32. Knapik, JJ, Meredith, CN, Jones, BH, Suek, L, Young, VR, and Evans, WJ. Influence of fasting on carbohydrate and fat metabolism during rest and exercise in men. J Appl Physiol 64: 1923–1929, 1988. 33. Lambert, GP, Lanspa, S, Welch, R, and Shi, X. Combined effects of glucose and fructose on fluid absorption from hypertonic carbohydrate-electrolyte beverages. J Exerc Physiol Online 11: 46–55, 2008. 34. Lecoultre, V, Benoit, R, Carrel, G, Schutz, Y, Millet, GP, Tappy, L, and Schneiter, P. Fructose and glucose co-ingestion during prolonged exercise increases lactate and glucose fluxes and oxidation compared with an equimolar intake of glucose. Am J Clin Nutr 92: 1071–1079, 2010. 35. Lee, MJC, Hammond, KM, Vasdev, A, Poole, KL, Impey, SG, Close, GL, and Morton, JP. Self-selecting fluid intake while maintaining high carbohydrate availability does not impair halfmarathon performance. Int J Sports Med 35: 1216–1222, 2014. 36. Maughan, RJ, Fenn, CE, and Leiper, JB. Effects of fluid, electrolyte and substrate ingestion on endurance capacity. Eur J Appl Physiol Occup Physiol 58: 481–486, 1989.

49. Rumessen, JJ and Gudmand-Høyer, E. Absorption capacity of fructose in healthy adults. Comparison with sucrose and its constituent monosaccharides. Gut 27: 1161–1168, 1986. 50. Roberts, JD, Tarpey, MD, Kass, LS, Tarpey, RJ, and Roberts, MG. Assessing a commercially available sports drink on exogenous carbohydrate oxidation, fluid delivery and sustained exercise performance. J Int Soc Sports Nutr 11: 8, 2014. 51. Rodriguez, NR, DiMarco, NM, and Langley, S. American dietetic association; Dietitians of Canada; american college of sports Medicine: Nutrition and athletic performance. Position of the american dietetic association, Dietitians of Canada, and the american college of sports Medicine: Nutrition and athletic performance. J Am Diet Assoc 109: 509–527, 2009. 52. Rose, S and Peters-Futre, EM. Ad libitum adjustments to fluid intake during cool environmental conditions maintain hydration status during a 3-day mountain bike race. Br J Sports Med 44: 430–436, 2010. 53. Rowlands, DS, Swift, M, Ros, M, and Green, JG. Composite versus single transportable carbohydrate solution enhances race and laboratory cycling performance. Appl Physiol Nutr Metab 37: 425– 436, 2012.

37. Moskowitz, HR. Ratio scales of sugar sweetness. Percept Psychophys 7: 315–320, 1970.

54. Running USA. Running USA’s Annual Marathon Report, 2013. Available at: http://www.runningusa.org/index.cfm? fuseaction=news.details&ArticleId=332&returnTo=annual-reports. Accessed November 20, 2013.

38. Murray, R. The effects of consuming carbohydrate-electrolyte beverages on gastric emptying and fluid absorption during and following exercise. Sports Med 4: 322–351, 1987.

55. Ryan, AJ, Bleiler, TL, Carter, JE, and Gisolfi, CV. Gastric emptying during prolonged cycling exercise in the heat. Med Sci Sports Exerc 21: 51–58, 1989.

39. O’Brien, WJ and Rowlands, DS. Fructose-maltodextrin ratio in a carbohydrate-electrolyte solution differentially affects exogenous carbohydrate oxidation rate, gut comfort, and performance. Am J Physiol Gastrointest Liver Physiol 300: G181–G189, 2011.

56. Sclafani, A. Starch and sugar tastes in rodents: An update. Brain Res Bull 27: 383–386, 1991.

40. O’Brien, WJ, Stannard, SR, Clarke, JA, and Rowlands, DS. Fructose— maltodextrin ratio governs exogenous and other CHO oxidation and performance. Med Sci Sports Exerc 45: 1814–1824, 2013. 41. Page, KA, Chan, O, Arora, J, Belfort-Deaguiar, R, Dzuira, J, Roehmholdt, B, Cline, GW, Naik, S, Sinha, R, Constable, RT, and Sherwin, RS. Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA 309: 63–70, 2013. 42. Park, OJ, Cesar, D, Faix, D, Wu, K, Shackleton, CH, and Hellerstein, MK. Mechanisms of fructose-induced hypertriglyceridaemia in the rat. Activation of hepatic pyruvate dehydrogenase through inhibition of pyruvate dehydrogenase kinase. Biochem J 282: 753–757, 1992.

57. Smith, JW, Zachwieja, JJ, Pe´ronnet, F, Passe, DH, Massicotte, D, Lavoie, C, and Pascoe, DD. Fuel selection and cycling endurance performance with ingestion of [13C] glucose: Evidence for a carbohydrate dose response. J Appl Physiol 108: 1520–1529, 2010. 58. Sole, CC and Noakes, TD. Faster gastric emptying for glucosepolymer and fructose solutions than for glucose in humans. Eur J Appl Physiol Occup Physiol 58: 605–612, 1989. 59. Stannard, SR, Hawke, EJ, and Schnell, N. The effect of galactose supplementation on endurance cycling performance. Eur J Clin Nutr 63: 209–214, 2009. 60. Sun, SZ and Empie, MW. Fructose metabolism in humans–what isotopic tracer studies tell us. Nutr Metab 9: 89, 2012. 61. Tappy, L and Leˆ, KA. Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 90: 23–46, 2010. VOLUME 29 | NUMBER 7 | JULY 2015 |

2069


Multiple Transportable Carbohydrates 62. Tarpey, MD, Roberts, JD, Kass, LS, Tarpey, RJ, and Roberts, MG. The ingestion of protein with a maltodextrin and fructose beverage on substrate utilisation and exercise performance. Appl Physiol Nutr Metab 38: 1245–1253, 2013. 63. Triplett, D, Doyle, JA, Rupp, JC, and Benardot, D. An isocaloric glucose-fructose beverage’s effect on simulated 100-km cycling performance compared with a glucose-only beverage. Int J Sports Nutr Exerc Metab 20: 122–131, 2010.

66. Wallis, GA and Wittekind, A. Is there a specific role for sucrose in sports and exercise performance?. Int J Sports Nutr Exerc Metab 23: 571–583, 2013. 67. Wood, IS and Trayhurn, P. Glucose transporters (GLUT and SGLT): Expanded families of sugar transport proteins. Br J Sports Med 89: 3– 9, 2003. 68. Wright, EM and Loo, DD. Coupling between Na+, sugar, and water transport across the intestine. Ann N Y Acad Sci 915: 54–66, 2000.

64. Wagenmakers, AJ, Brouns, F, Saris, WHM, and Halliday, D. Oxidation rates of orally ingested carbohydrates during prolonged exercise in men. J Appl Physiol 75: 2774–2780, 1993.

69. Zittel, TT, Rothenhofer, I, Meyer, JH, and Raybould, HE. Small intestinal capsaicin-sensitive afferents mediate feedback inhibition of gastric emptying in rats. Am J Physiol 267: G1142–G1145, 1994.

65. Wallis, GA, Rowlands, DS, Shaw, C, Jentjens, RL, and Jeukendrup, AE. Oxidation of combined ingestion of maltodextrins and fructose during exercise. Med Sci Sports Exerc 37: 426–432, 2005.

70. Zukerman, S, Glendinning, JI, Margolskee, RF, and Sclafani, A. T1R3 taste receptor is critical for sucrose but not Polycose taste. Am J Physiol 296: R866–R876, 2009.

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