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SYSTEMATIC REVIEW Effect of Glycemic Index of a Pre-exercise Meal on Endurance Exercise Performance: A Systematic Review and Meta-analysis Catriona A. Burdon1,2 • Inge Spronk3 • Hoi Lun Cheng1,4,5 • Helen T. O’Connor1,6 � Springer International Publishing Switzerland 2016 Abstract Background Low glycemic index (GI) pre-exercise meals may enhance endurance performance by maintaining eug- lycemia and altering fuel utilization. However, evidence for performance benefits is equivocal. Objective To evaluate the effect of a low GI (LGI) versus a high GI (HGI) pre-exercise meal on endurance perfor- mance using meta-analyses. Methods Data sources included MEDLINE, SPORTDis- cus, AUSPORT, AusportMed, Web of Science, and Sco- pus. Eligibility criteria were randomized, crossover trials with an endurance exercise (C60 min) component, e.g., time trial (TT), time to exhaustion (TTE) test, or sub- maximal bout followed by TT or TTE. Participants were healthy, active individuals aged C16 years. Interventions included a LGI (B55) and HGI (C70) meal ingested 30–240 min before exercise. Study quality was assessed using an adapted version of the validated Downs and Black tool. Effect size (ES) and 95 % confidence interval were calculated for each study and pooled according to perfor- mance test type and whether exogenous carbohydrate (CHO) was given during exercise. Potential effect modi- fiers including exercise duration, pre-exercise meal timing, glycemic load (GL), and fitness were assessed using meta- regression. Results The search netted 3431 citations with 19 studies eligible for inclusion (totaling 188 participants; 91 % male; VO2max: [50 ml/kg/min). Meals with 0.18–2 g CHO/kg body mass, and a mean GI and glycemic load of 82 (GL: 72) and 35 (GL: 32) for HGI and LGI, respec- tively, were given between 30 and 210 min before exercise. All test types without CHO ingestion during exercise showed slightly improved performance with LGI, but no significant pooled effects were observed (ES: -0.17 to -0.36; p[ 0.05). Studies where exoge- nous CHO was ingested during exercise showed con- flicting results (ES: -0.67 to 0.11; p = 0.04 to 0.94). No significant relationship was observed with any of the effect modifiers (p[ 0.05). No consistent metabolic responses (glucose, insulin, lactate, respiratory exchange ratio) during exercise were observed with either meal type. Limitations There were small numbers of studies within each exercise testing protocol and limited statistical power within studies. Pre-exercise meal timing, GL, meal com- position and participant fitness varied across studies, lim- iting the capacity to assess the influence of these factors on study outcomes. Conclusion There was no clear benefit of consuming a LGI pre-exercise meal for endurance performance regardless of carbohydrate ingestion during exercise. & Helen T. O’Connor helen.oconnor@sydney.edu.au 1 Discipline of Exercise and Sport Science, Faculty of Health Sciences, The University of Sydney, 75 East Street, Lidcombe, Sydney, NSW 2141, Australia 2 School of Medicine, University of Wollongong, Wollongong, NSW, Australia 3 Wageningen University, Wageningen, The Netherlands 4 Academic Department of Adolescent Medicine, The Children’s Hospital at Westmead, Westmead, Sydney, NSW, Australia 5 Discipline of Child and Adolescent Health, Sydney Medical School, The University of Sydney, Westmead, Sydney, NSW, Australia 6 Charles Perkins Centre, The University of Sydney, Camperdown, Sydney, NSW, Australia 123 Sports Med DOI 10.1007/s40279-016-0632-8 Key Points Meta-analysis did not find significantly improved endurance exercise performance with a low glycemic index (LGI) pre-exercise meal, regardless of exogenous carbohydrate (CHO) ingestion during exercise. However, a small, non-significant performance benefit across all exercise test types was observed after a LGI meal when no CHO was ingested during exercise. Maintenance of CHO availability (glucose or glycogen) is one of the main reasons a LGI pre- exercise meal is proposed to enhance endurance performance. As most, if not all, athletes have regular access to exogenous CHO during competitive events, it would seem that exogenous CHO ingestion would replace the need for a LGI pre-exercise meal. In prolonged exercise situations where access to exogenous CHO is restricted, limited (e.g., military rescue situations or in endurance events for athletes with a disability where access to exogenous CHO may be logisitically difficult) or not well tolerated (gastrointestinal upset), a LGI pre-exercise meal may be theoretically useful. Further research evidence addressing this question is warranted. 1 Introduction Consumption of carbohydrate (CHO) or a CHO-based meal before exercise is a widely accepted practice for endurance athletes. It is used not only to satisfy hunger and help meet daily nutrient requirements, but it is also important for supporting the energy needs of exercise and optimizing performance [1]. Pre-exercise CHO ingestion can increase glycogen stores and/or blood glucose levels, and is known to increase CHO utilization during exercise [2]. The majority of studies examining pre-exercise CHO con- sumption have demonstrated null to beneficial effects on endurance performance when compared to exercising in the fasted state [1–3]. One of the more controversial aspects of the pre-exer- cise meal has been the glycemic index (GI). The GI is determined by comparing the post-prandial blood glucose response of a food/meal to that of glucose (which has a reference GI value of 100). A low GI (LGI) meal is absorbed slowly from the gut, such that the rise in glucose and insulin are blunted in comparison to a high GI (HGI) meal [4, 5]. Various techniques can be used to manipulate the GI of a meal. These include altering the macronutrient composition, form or particle size (e.g., liquid or solid), cooking method, and, more commonly, the type of CHO within the meal [4, 6, 7]. Interest in manipulating the GI of pre-exercise meals was initially driven by concerns that pre-exercise CHO consumption can induce a nadir in blood glucose levels, and potentially hypoglycemia, during the initial stages (*30 min) of endurance exercise [8]. Early studies in the area (predominantly from the 1980s) explored simple versus complex CHO meals, as GI was not yet established as a scientific concept [9–11]. Outcomes from these studies were equivocal, although practical advice to athletes before and during the early 1990s often included avoidance of simple CHO or sugars in the pre- exercise period [12]. Simple sugars were considered most likely to induce a nadir in blood glucose levels, as they were believed to be linked with higher insulin secretion [13]. Over the past two decades, the classification of CHO based on GI became more widely accepted, and research on LGI foods confirmed its effects on attenuating post- prandial insulin levels [14, 15]. This was recognized as potentially beneficial for maintaining euglycemia during exercise, and the sustained release of slowly-digested LGI CHO was seen as attractive for maintaining CHO avail- ability, particularly in the later stages of prolonged exercise [16]. Attenuation of post-prandial insulinemia was also believed to facilitate free fatty acid release and fat oxida- tion, which may reduce muscle glycogen depletion [4]. Despite these purported benefits, studies comparing HGI versus LGI pre-exercise meals on exercise performance have yielded mixed results and several critical reviews report that the evidence is inconclusive [1, 17, 18]. Smallsample size is often identified as a limitation in these reviews, and a meta-analysis in this instance would be advantageous for providing greater power to detect ergo- genic effects of LGI pre-exercise meals. The provision of exogenous CHO during exercise (which alters CHO availability and fuel utilization) in some studies further complicates interpretation of research find- ings [17]. Additionally, research has demonstrated that glycemic response to a CHO food is not only dependent on the GI value itself, but also the total amount of CHO ingested [19, 20]. This combined effect, known as the glycemic load (GL), has been shown to explain*90 % of the variability in the blood glucose response [21]. Pre-ex- ercise GL has only been assessed in one endurance exercise study which showed a null effect on performance [22]. However, as most studies examining meal GI typically report CHO content, it is possible to undertake a more comprehensive evaluation of GL using existing literature. The primary aim of this study was to conduct a sys- tematic review and meta-analysis of randomized crossover trials in trained/highly-trained participants to examine how C. A. Burdon et al. 123 the GI of a pre-exercise meal affects endurance perfor- mance. A secondary aim was to investigate the influence of potential effect modifiers including the GL, time between meal ingestion, and exercise onset (pre-exercise meal timing), CHO ingestion during exercise and participant fitness. Clarification of the potential benefit of LGI meals prior to exercise will enable athlete recommendations to be more confidently determined. 2 Methods 2.1 Search Strategy This review was conducted in accordance with the Pre- ferred Reporting Items for Systematic Reviews and Meta- analysis (PRISMA) Statement [23]. A systematic search was conducted from the earliest record using the databases MEDLINE (via OvidSP), SPORTDiscus (via EBSCOhost), AUSPORT and AusportMed (via Informit), Web of Sci- ence, and Scopus. The search strategy (Fig. 1) combined terms covering the areas of glycemic index (glycemic index; glycaemic index; GI) and sport performance (per- formance; exercise; physical activity; sport; competition; event). Reference lists of included studies, review articles, and publications from known authors in the research area were hand-searched. The search was performed by one reviewer (IS). After removal of duplicates and exclusion by title and abstract, two reviewers (IS and CB) independently evaluated studies for inclusion with disagreements resolved via discussions with a third reviewer (HOC). Reviewers were not masked to study titles or authors. Papers in lan- guages other than English were translated by a native speaker, and only excluded if a translation was not possi- ble. The initial search was conducted in February 2014 and updated in January 2015. 2.2 Eligibility Criteria To be included, studies were required to have a crossover design where participants were randomized to receive a HGI and LGI meal 30 to 240 min prior to exercise. This time frame was informed by current guidelines for pre- event CHO consumption of 1–4 h prior to exercise [24]. As we were aware a priori that meals fed as little as 30 min prior to exercise were used to explore the risk of hypo- glycemia (which may compromise endurance perfor- mance), we set the lower limit for consumption at 30 min prior to exercise. This was also practically a feasible minimum time for a meal to be consumed. Definitions of C70 for HGI and B55 for LGI were used as exclusion cut points, in accordance with the international tables of GI and GL values [14]. Studies using meals that were\5 GI units outside these cut points were included if the GI values of the meals were C15 units apart, emulating the above- mentioned international cut-offs for HGI and LGI. Original and complete research only was included, therefore review and opinion articles and abstracts were excluded, and non- randomized trials were excluded to maximize study quality. Study participants needed to be physically active, heal- thy, able-bodied, and C16 years of age. Where age range was not provided, studies were accepted if the mean age minus one standard deviation (SD) was C16 years. Studies were excluded if participants had a disability (e.g., spinal cord injury), or any condition that affected performance (e.g., chronic obstructive pulmonary disease) or CHO metabolism (e.g., diabetes). Studies needed to include some form of endurance exercise (C60 min) as part of or in combination with a performance test, for example time trial (TT), submaximal bout followed by time trial (sub- max ? TT), time to exhaustion (TTE), submaximal bout followed by TTE (submax ? TTE), or incremental TTE protocols. 2.3 Data Extraction Participant characteristics (age; sex; source population; fitness/aerobic capacity), test conditions (environmental conditions; food/drink consumed during exercise; exercise protocol and duration; performance test type), intervention characteristics (meal GI and CHO content; meal compo- sition; pre-exercise meal timing) and performance Search terms: performance, exercise, physical activity, sport, competition or event n = 1,184,900 Search terms: GI, glycemic index, glycaemic index n = 158,958 Articles screened (after duplicate removal) n = 3,431 Full-text articles assessed for eligibility n = 112 Articles excluded (after title and abstract review) n = 3,319 Hand searched articles n = 8 Studies included in qualitative synthesis n = 19 Full-text articles excluded n = 101 Irrelevant: n = 25 Not RCT or crossover design: n = 12 Under 16 years: n = 2 Sedentary participants: n = 1 Performance not measured: n = 20 Meal consumption <30 min or >240 min before exercise: n = 9 or GI difference <15: n = 5 No GI reported for meals: n = 1 Not a single pre-exercise meal: n = 2 Not an endurance exercise protocol: n = 2 Review, abstract or thesis: n = 22 Studies included in quantitative synthesis (meta-analyses) n = 19 Fig. 1 Flowchart of the study selection process. HGI high glycemic index, LGI low glycemic index, RCT randomized controlled trial Effect of Glycemic Index of a Pre-exercise Meal on Endurance Performance 123 outcomes were extracted by one reviewer (IS), and checked independently by another (HLC). For studies that tested more than two pre-exercise meals, the two with the highest and lowest GI values were selected. GL was calculated (GI 9 CHO content in grams) from data reported in each manuscript. As CHO content of meals needed to be rea- sonably well matched for the study to be included, dis- crepancies in GL were primarily attributed to differences in GI. A range of GLs were observed across the included studies, enabling its impact to be qualitatively assessed. Descriptive summary data on participants’ metabolic response to the meal were also extracted. Where necessary, SD was calculated from standard errors. To facilitate comparison between studies, exercise duration and aerobic capacity were calculated from available data. For studies that only presented data graphically, mean and SD were estimated in duplicate using a graduated measure. 2.4 Assessment of Methodological Quality Study quality was assessed by two reviewers (CB and IS) using a modified Downs and Black checklist, with a maximum of 21 points [25]. Disagreements were resolved by discussion with a third reviewer (HOC). Quality items not relevant to a two-visit, crossover, randomized controlled trial design (i.e., patients lost to follow-up stated; representative facilities; data dredging;different follow-up lengths; consistent population recruited and time frame; randomization concealed; accounting for subjects lost to follow-up; and adjusting for confounders) were removed. For the item assessing whether study sam- ples were representative of trained populations, maximal oxygen consumption ( _VO2max) thresholds of [55 and [40 ml/kg/min were used for men and women, respec- tively [26]. Populations were described as well trained if _VO2max was[65 ml/kg/min for men and[55 ml/kg/min for women [26]. Assessment of participant blinding was expanded to two quality items, in order to assess blinding to both meal GI and performance tests. The statistical power of each study was evaluated via power calculations using the effect size (G*Power version 3.1, Franz Faul, Universita¨t Kiel, Germany) [27]. No studies were eliminated and no additional sub-group analyses were undertaken on the basis of methodological quality. Assessment of confounding was improved via three additional items. These assessed whether studies controlled for: (1) participant glucose tolerance; as well as (2) diet; and (3) exercise in the 24 h prior to the experi- mental days. Correspondingly, the item relating to bias/compliance was attributed an additional point to evaluate participant adherence to diet and exercise control guidelines. This additional point was only awarded if a study reported evidence of compliance (via food and exercise diaries or other tool to quantify diet and exercise in the 24 h prior to experimental days). 2.5 Data Analyses Comprehensive Meta-Analysis Version 3 (Englewood, NJ, USA) was used to calculate the standardized mean differ- ence or effect size (ES) and 95 % confidence interval (95 % CI) for each study, and to combine data using the random effects model for meta-analysis. Separate meta- analyses were conducted for each exercise performance test category, and for studies that did not provide CHO during exercise. Results were summarized using forest plots, with a negative ES representing an ergogenic benefit of a LGI meal and vice versa. Heterogeneity between studies was assessed using I2 [28]. The weighted mean difference (WMD) for relative change in performance was calculated as the mean of the percent change between the HGI and LGI trials, with each study weighted according to sample size. No assessment of publication bias was undertaken as there were too few studies within each per- formance test category [29]. Studies within the forest plots were arranged from smallest to largest GL differences between the HGI and LGI pre-exercise meals. Meta-re- gression was undertaken to examine whether variations in GL, pre-exercise meal timing, and participant fitness between studies influenced the strength of individual study outcomes. 3 Results 3.1 Identification and Selection of Studies Upon completion of the initial search and removal of duplicates, 3431 citations were available for review. After elimination of papers based on the eligibility criteria, 19 articles were included (Fig. 1). 3.2 Study Characteristics Participant and meal characteristics for each study are presented in Table 1. Across the 19 included studies, sample size ranged from six to 34. Participant age ranged between 21 and 33 years. Seventeen studies recruited only males, and two included participants of both sexes. This equated to a combined total of 188 participants, with a 91 % male representation. Trained and well trained par- ticipants were used in 15 and two studies, respectively, with _VO2max not reported in two studies [30, 31]. All of the highly trained participants were male. C. A. Burdon et al. 123 T a b le 1 P ar ti ci p an t an d m ea l ch ar ac te ri st ic s o f in cl u d ed st u d ie s S tu d y P ar ti ci p an t ch ar ac te ri st ic s M ea l ch ar ac te ri st ic s P re -e x er ci se ti m e (m in ) n A g e (y ea rs )a P o p u la ti o n V O 2 m a x (m l/ k g /m in )a C H O (g / k g ) H ig h g ly ce m ic in d ex L o w g ly ce m ic in d ex B en n et t et al . [3 8 ] 1 0 M 4 F M : 2 7 .2 ± 8 .0 F : 2 2 .5 ± 4 .4 T ra in ed so cc er p la y er s M : 5 5 .8 ± 5 .5 F : 5 4 .6 ± 4 .8 1 .5 In st an t m as h ed p o ta to es , w h it e b re ad (G I: 7 5 ) R ed le n ti ls , h o n ey , S as k at o o n b er ri es (G I: 3 6 ) 1 2 0 B u rk e et al . [3 3 ] 6 M 2 2 .8 ± 2 .3 W el l- tr ai n ed cy cl is ts 6 8 .6 ± 3 .8 2 In st an t m as h ed p o ta to (G I: 8 7 ) L ig h tl y co o k ed p as ta (G I: 3 7 ) 1 2 0 C h en et al . [2 2 ] 8 M 2 4 .3 ± 2 .2 T ra in ed ru n n er s 5 5 .9 ± 1 .9 1 .5 P o ta to , so y m il k , h am , w h it e su g ar , ra w eg g (G I: 7 9 ) A p p le , h am , m ac ar o n i, to m at o sa u ce (G I: 4 0 ) 1 2 0 C h en et al . [3 4 ] 8 M 2 8 .6 ± 2 .7 T ra in ed ru n n er s 5 8 .5 ± 1 .6 1 .5 Ja sm in e ri ce , eg g , h am , sl ic ed p ar sn ip s, ca n n ed ly ch ee s, fi sh st ic k s, o ra n g e so d a (G I: 8 3 ) M u n g b ea n th re ad n o o d le s, ch ic k en b ro th , h ar d b o il ed eg g , fi sh st ic k s, g re en p ea s, so y m il k (G I: 3 6 ) 1 2 0 D eM ar co et al . [3 7 ] 1 0 M 3 0 .7 ± 4 .3 T ra in ed cy cl is ts 6 1 .2 ± 5 .2 1 .5 C o rn fl ak es , b an an a, an d m il k (G I: 6 9 ) A ll B ra n , ap p le , u n sw ee te n ed y o g h u rt (G I: 3 6 ) 3 0 F eb b ra io an d S te w ar t [4 3 ] 6 M 2 9 ± 2 T ra in ed cy cl is ts 6 2 .1 ± 3 .6 1 In st an t m as h ed p o ta to (G I: 8 0 ) L en ti ls (G I: 2 9 ) 4 5 F eb b ra io et al . [4 2 ] 8 M 2 6 ± 6 T ra in ed cy cl is ts 6 0 .5 ± 5 1 In st an t m as h ed p o ta to (G I: 8 0 ) M u es li (G I: 5 2 ) 3 0 H u lt o n et al . [3 0 ] 9 M 2 1 ± 3 A ct iv e su b je ct s N o t re p o rt ed 2 L u co za d e, as k as h ri ce , ch ic k en b re as t, to m at o - b as ed sa u ce (G I: 8 0 ) A p p le ju ic e, b as m at i ri ce , ch ic k en b re as t, to m at o - b as ed sa u ce (G I: 4 4 ) 2 1 0 L it tl e et al . [3 2 ] 7 M 2 3 .3 ± 3 .8 T ra in ed at h le te s (m ix ed ) 5 6 .7 ± 5 .0 1 .3 In st an t m as h ed p ota to , eg g w h it es , k et ch u p (G I: 8 1 ) B o il ed re d le n ti ls (G I: 2 9 ) 1 8 0 L it tl e et al . [3 9 ] 1 3 M 2 2 .8 ± 3 .2 T ra in ed at h le te s (m ix ed ) 5 5 .4 ± 4 .3 1 .5 In st an t m as h ed p o ta to , w h it e b re ad , eg g w h it es (G I: 7 6 ) R ed le n ti ls (G I: 2 6 ) 1 2 0 M o o re et al . [4 0 ] 8 M 2 9 .4 ± 6 .4 T ra in ed cy cl is ts 5 8 .2 ± 1 0 .1 1 C o rn fl ak es , se m i- sk im m il k (G I: 7 2 ) A ll b ra n , se m i- sk im m il k (G I: 3 0 ) 4 5 M o o re et al . [4 1 ] 1 0 M 2 8 ± 6 T ra in ed cy cl is ts 5 8 .2 ± 1 0 .1 1 C o rn fl ak es , se m i- sk im m il k (G I: 7 2 ) A ll b ra n , se m i- sk im m il k (G I: 3 0 ) 4 5 R el ji c et al . [3 1 ] 2 0 M 1 4 F M : 3 2 .7 ± 9 F : 2 6 .6 ± 5 .1 T ra in ed ru n n er s N o t re p o rt ed 0 .1 8 P o w er ad e (g lu co se an d m al to d ex tr in ) (G I: 1 0 0 ) C ap ri S u n S p o rt d ri n k (f ru it sw ee te n er an d w h ea t d ex tr in ) (G I: 4 0 ) 3 0 S p ar k s et al . [4 4 ] 8 M 2 2 .7 ± 1 .4 W el l- tr ai n ed cy cl is ts 6 7 .9 ± 2 .8 1 In st an t m as h ed p o ta to (G I: 8 0 ) L en ti ls (G I: 2 9 ) 4 5 T h o m as et al . [1 6 ] 8 M 2 9 ± 6 T ra in ed cy cl is ts 6 2 .5 ± 3 .7 1 B ak ed p o ta to (G I: 9 8 ) B o il ed le n ti ls (G I: 2 9 ) 6 0 T h o m as et al . [4 8 ] 6 M 2 5 ± 5 T ra in ed cy cl is ts * 6 0 (4 .2 ± 0 .5 L /m in ) 1 P o ta to fl ak es (G I: 1 0 0 ) B ra n ce re al (G I: 3 0 ) 6 0 Effect of Glycemic Index of a Pre-exercise Meal on Endurance Performance 123 The HGI and LGI pre-exercise meals provided similar amounts of energy (HGI: 2228 ± 808; LGI: 2321 ± 793 kJ), CHO (HGI: 90.6 ± 31.7; LGI: 91.3 ± 31.6 g), protein (HGI: 20.1 ± 8.8; LGI: 24.6 ± 10.5 g), and fat (HGI: 9.1 ± 7.0; LGI: 9.0 ± 6.9 g). The CHO content of pre-exercise meals varied from 0.18 to 2 g/kg body mass. Mean GI was 82 (range 69–100) and 35 (range 26–52) for the HGI and LGI meals, respectively. This corresponded to a mean GL of 72 (range 14–124) for the HGI meals and 32 (range 5–59) for the LGI meals. Mean time lapse between the pre-exercise meal and onset of exercise was 95 min (range 30–210 min). Timing of pre-exercise meals was: 30 (n = 3); 45 (n = 4); 60 (n = 2); 120 (n = 7); 180 (n = 2); and 210 min (n = 1). Additional CHO was given during exercise in five studies; two with a LGI or a HGI CHO as per the pre-exercise meal [31, 32], one with a radio-labeled glucose solution [33], and two with a commercial CHO- electrolyte drink [34, 35]. GI values for the commercial drinks were unavailable, but were treated as high due to their glucose content [36]. A summary of the exercise protocols used for each study is presented in Table 2. Four different protocols were used to measure performance across the 19 studies: TT (n = 5); submax ? TT (n = 9); TTE (n = 4); and submax ? TTE (n = 1). Total exercise duration ranged from 65 to 150 min, and was conducted on either a cycle ergometer (n = 9) or treadmill (n = 10). Meta-regression was carried out on each of these different exercise protocols except submax ? TTE as only one study had this type of design [37]. 3.3 Meta-analysis: Time-Trial Performance Tests Four studies used a TT protocol without any additional CHO consumption during exercise (Fig. 2) [38–41]. Sig- nificantly better performance was reported for the LGI trial in two of the four papers [40, 41]. Upon pooling of these studies, there was no significant effect of a LGI meal on TT performance (ES: -0.18; 95 % CI -0.58 to 0.22; p = 0.37; I2 = 0 %). The WMD represented a 0.7 % improvement with a LGI meal, with percent change rang- ing from -1.8 to 3.2 %. One study provided CHO during exercise, showing an ES of -0.04 (95 % CI -1.02 to 0.95; p = 0.94) and a 1.4 % WMD favoring a LGI meal [32]. 3.4 Meta-analysis: Submaximal Plus Time-Trial Performance Tests A total of six studies used a submax ? TT protocol with- out providing CHO during exercise (Fig. 3) [22, 30, 42–45]. Of these, five favored a LGI meal for superior performance [22, 30, 43–45], with only one reporting a significant effect of a LGI meal [45]. TheT a b le 1 co n ti n u ed S tu d y P ar ti ci p an t ch ar ac te ri st ic s M ea l ch ar ac te ri st ic s P re -e x er ci se ti m e (m in ) n A g e (y ea rs )a P o p u la ti o n V O 2 m a x (m l/ k g /m in )a C H O (g / k g ) H ig h g ly ce m ic in d ex L o w g ly ce m ic in d ex W o n g et al . [4 5 ] 8 M 3 3 ± 1 .7 T ra in ed ru n n er s 6 3 ± 1 .8 1 .5 B ak ed p o ta to , m ar g ar in e, to m at o sa u ce , lo w fa t p ro ce ss ed ch ee se , ri ce cr is p ie s, so ft d ri n k (G I: 7 7 ) C o o k ed m ac ar o n i, ap p le sl ic es , ca n n ed ch ic k p ea s, lo w fa t p ro ce ss ed ch ee se , fr u it -fl av o re d y o g h u rt , ap p le ju ic e (G I: 3 7 ) 1 2 0 W o n g et al . [4 7 ] 9 M 2 4 ± 2 .4 T ra in ed ru n n er s 5 8 .4 ± 1 .5 1 .5 Ja sm in e ri ce , eg g , h am , sl ic ed p ar sn ip s, ca n n ed ly ch ee s, fi sh st ic k s, o ra n g e so d a (G I: 8 3 ) M u n g b ea n th re ad n o o d le s, ch ic k en b ro th , h ar d b o il ed eg g , fi sh st ic k s, g re en p ea s, so y m il k (G I: 3 6 ) 1 2 0 W u an d W il li am s [4 9 ] 8 M 2 8 .9 ± 1 .5 T ra in ed ac ti v e su b je ct s 6 0 .6 ± 1 .5 2 C o rn fl ak es , sk im m il k , w h it e b re ad , ja m , L u co za d e (G I: 7 7 ) B ra n fl ak es , sk im m il k , ca n n ed p ea ch es , ap p le , ap p le ju ic e (G I: 3 7 ) 1 8 0 C H O ca rb o h y d ra te , G I g ly ce m ic in d ex , M m al e, F fe m al e, V O 2 m a x m ax im u m o x y g en u p ta k e a V al u es ar e m ea n ± st an d ar d d evia ti o n C. A. Burdon et al. 123 pooled effect across the six studies was not significant (ES: -0.17; 95 % CI -0.55 to 0.22; p = 0.40; I2 = 0 %). The WMD was 1.3 % favoring the LGI trial, with percent change ranging from -6.9 to 6.4 %. The opposite pattern was observed in the three studies that provided CHO dur- ing the submax ? TT protocol [34, 46, 47]. All three showed slightly better performance with a HGI meal, but the pooled effect was non-significant (ES: 0.11; 95 % CI - 0.44 to 0.65; p = 0.70; I2 = 0 %). This equated to a 0.9 % WMD favoring the HGI trial, and percent change ranging from -1.0 to -0.8 %. 3.5 Meta-analysis: Time-to-Exhaustion Performance Tests Three studies used a TTE design without providing CHO during exercise (Fig. 4) [16, 48, 49], two of which reported a significant performance benefit after the LGI meal [16, 49]. However, when these studies were pooled, the performance improvement with LGI meals was not sig- nificant (ES: -0.36; 95 % CI -0.93 to 0.22; p = 0.22; I2 = 0 %) (Fig. 4). This equated to a WMD of 5.0 % in favor of LGI meals, and a percentage mean change of -4.4 Table 2 Exercise protocols of included studies Study Food/drink during exercise Exercise modality Environmenta Protocol Performance test Exercise duration (min)Content (volume) Timing (min into exercise) Bennet et al. [38] N/A N/A Running Not reported 5 9 15 min intermittent varied intensity 5 9 1 min sprints 90 Burke et al. [33] Rest: 10 % CHO 1 g/kg (4 ml/kg) During: 3.3 ml/kg Rest and 20 min Cycling Not reported 70 % VO2max 15 min (300 kJ) TT 135 Chen et al. [22] N/A N/A Running 20–21 ± 1 �C; 61–62 ± 2 % RH 60 min at 70 % VO2max 10 km TT 112 Chen et al. [34] 6.6 % CHO (2 ml/kg) 2.5 km Running 21.3 ± 0.6 �C; 62.0 ± 2.2 % RH 5 km at 70 % VO2max 16 km TT 92 DeMarco et al. [37] Water (150 ml) 20 min Cycling 21 ± 1 �C 120 min at 70 % VO2max TTE 100 % VO2max [120 Febbraio and Stewart 1996 [43] Water (250 ml) 15 min Cycling 20–22 �C 120 min at 70 % VO2max 15 min TT 135 Febbraio et al. [42] Water (250 ml) 15 min Cycling 20–22 �C 120 min at 70 % VO2max 30 min TT 150 Hulton et al. [30] Water (5 ml/kg) 45 min (15 min rest) Running Not reported 4 9 22.5 min varied intensity, 15 min rest 1 km TT *94 Little et al. [32] HGI or LGI snack (0.25 g/kg CHO) 45 min Running Not reported 5 9 15 min intermittent varied intensity 5 9 1 min sprints 90 Little et al. [39] Water ad libitum (matched) 15 min Running Not reported 5 9 15 min intermittent varied intensity 5 9 1 min sprints 90 Moore et al. [40] Water ad libitum (equal both trials) N/A Cycling 22 ± 2 �C; 48 ± 5 % RH N/A 40 km TT 95 Moore et al. [41] Not reported N/A Cycling 20–22 �C; 48 ± 5 % RH N/A 40 km TT 96 Reljic et al. [31] HGI or LGI drink (250 ml 9 2) 30 and 60 min Running 20–22 �C; 50–60 % RH 90 % lactate threshold TTE 80 Sparks et al. [44] Water (400 ml) 15 min Cycling 21 �C 50 min at 67 % VO2max 15 min TT 65 Thomas et al. [16] Water (120 ml) 15 min Cycling 23 ± 1 �C; 60–65 %RH 67 % VO2max TTE 117 Thomas et al. [48] Water (120 ml) 15 min Cycling 23 ± 1 �C; 60–65 %RH 67 % VO2max TTE 101 Wong et al. [45] Water (125 ml) 2.5 km Running 22.1 ± 0.4 �C; 64 ± 2 % RH 5 km at 70 % VO2max 16 km TT 99 Wong et al. [47] 6.6 % CHO 2 ml kg-1 at rest Rest and 2.5 km Running Not reported 5 km 70 % VO2max 16 km TT 92 Wu and Williams [49] Water (2 ml kg-1) 15 min Running Not reported 70 % VO2max TTE 109 CHO carbohydrate, HGI high glycemic index, LGI low glycemic index, N/A not applicable, RH relative humidity, TT time trial, TTE time to exhaustion, VO2max maximum oxygen uptake a Values are mean ± standard deviation or range Effect of Glycemic Index of a Pre-exercise Meal on Endurance Performance 123 to 17.1 %. One study [31] provided a CHO drink during exercise (consistent with the GI value of the pre-test meal), and found a significant 7.7 % performance benefit after the LGI meal (ES: -0.49; 95 % CI -0.97 to -0.02; p = 0.04). Only one study used a submax ? TTE protocol [37], which reported significantly better performance after consumption of a LGI meal. This contrasted with the cal- culated effect size which showed a non-significant 36.1 % improvement in performance after the LGI meal (ES: -0.67, 95 % CI -1.57 to 0.23; p = 0.13). 3.6 Potential Effect Modifiers: Glycemic Load, Pre-exercise Meal Timing, and Fitness Qualitative evaluation of forest plots (Figs. 2, 3, 4), where studies were arranged from lowest to highest GL differences between the HGI and LGI meals, showed no consistent performance patterns with varying GL. This is consistent with results from the meta-regression (Fig. 5) where no association was observed between performance effect and meal GL differences across the studies (coefficient: 0.01; standard error: 0.01; p = 0.31). Similarly, no significant relationships were found for pre-exercise meal timing (co- efficient: 0.00; standard error: 0.00; p = 0.38) and partici- pant fitness (coefficient: -0.01; standard error: 0.03; p = 0.74), even when studies without CHO provision during exercise were analyzed independently (data not shown). 3.7 Metabolic Responses During Exercise The response of the metabolic variables during exercise is summarized in Table 3. All studies measured blood glu- cose and observed normal values at rest prior to meal consumption. Study n ES (95% CI) p value TT (no CHO during exercise) ] 8 29 - - ) ] 10 29 - - ) ] 14 31 (- ) ] 13 56 - - ) Pooled effect (no CHO) - - ) TT (CHO during exercise) ] 40 - - ) - - Favors HGI Fig. 2 Forest plot showing HGI vs. LGI pre-exercise meal effects on performance in time trials (TT) without (n = 4; white squares) and with (n = 1; gray square) CHO ingestion during exercise. Studies are arranged according to GL differences between the HGI and LGI meals and size varies with subject number. Diamond represents the pooled effect from studies without CHO ingestion during exercise. CHO carbohydrate, CI confidence interval, Diff, difference, ES effect size, GL glycemic load, HGI high glycemic index, LGI low glycemic index ES (95% CI) p value Submax+TT (no CHO during exercise) Febbraio ] 8 20 (- ) ] 8 36 - - Febbraio ] 6 - - ) ] 8 38 - - ) ] 8 41 - - ) Hulton ] 8 52 - - ) Pooled effect (no CHO) - - ) Submax+TT (CHO during exercise) ] 9 43 (- ) ] 8 (- ) ] 6 (- ) Pooled effect (with CHO) (- ) - - Favors HGI Study n Fig. 3 Forest plot showing HGI vs. LGI pre-exercise meal effects on performance in submaximal exercise plus time trial (submax ? TT) studies without (n = 6; white squares) and with (n = 3; gray squares) CHO ingestion during exercise. Studies are arranged according to GL differences between the HGI and LGI meals and size varies with subject number. Diamonds represent the pooled effects from studies without and with CHO ingestion during exercise. CHO carbohydrate, CI confidence interval, Diff, difference, ES effect size, GL glycemic load, HGI high glycemic index, LGI low glycemic index C. A. Burdon et al. 123 3.7.1 No Carbohydrate (CHO) Consumed During Exercise Of the 14 studies that did not provide CHO during exercise, seven reported no difference in blood glucose between the HGI and LGI trials, six found lower blood glucose with a HGI meal at some point during exercise, and one reported superior blood glucose maintenance with a LGI meal. Circulating insulin was measured in 13 studies, with 11 reporting no dif- ference between the trials, and two(both with a short pre- exercise meal timing of 30 and 45 min) showing higher insulin in the first 20 min of exercise after the HGI meal [37, 44]. A total of 12 studies measured blood lactate. Ten of these showed no difference between the HGI and LGI trials, one reported higher levels throughout exercise after a HGI meal [22], and one found significantly higher lactate at the beginning andmid-way through exercise on theHGI trial [16]. Free fatty acid (FFA) concentration was measured in nine studies, with three finding no difference between trials; the remaining six observed lower FFA with a HGI meal throughout or at some point during exercise. Respiratory exchange ratio (RER) was measured in 12 studies; four reported no difference between trials. Six studies observed higher and two observed lower RER throughout or at some point during exercise after a HGI meal. Carbohydrate and fat oxidation were measured in 11 and 10 studies respectively, with four reporting no differ- ence in oxidation rates of either fuel. Higher CHO oxida- tion in five and lower CHO oxidation in two studies were observed during the HGI trial. Fat oxidation was lower in four and higher in two studies after the HGI meal. 3.7.2 CHO Consumed During Exercise The five studies where CHO was given as a part of the performance test protocol found no differences between HGI and LGI trials for circulating insulin, blood lactate, FFA, RER, or CHO and fat oxidation during exercise [31–35]. One study by Reljic et al. reported higher blood glucose levels during exercise after the LGI meal [31]. 3.8 Methodological Quality Methodological quality of the included studies was mixed (Table 4). Studies scored an average of 14 points out of 21 (range 11–17), with excellent reporting of some items. Reporting of participant description, adverse events, and actual probability values was poor. Only four [16, 22, 40, 48] of the 19 studies blinded participants to the meal, 12 [16, 22, 30, 32, 33, 37–41, 45, 48] to exercise performance as an outcome, and six [22, 31, 32, 38, 40, 45] blinded researchers. Two [33, 40] studies verified compli- ance with pre-trial instructions; however, another nine [22, 30, 32, 34, 39, 41, 44, 45, 47] reported checking compliance but did not report results. Confounding factors (glucose tolerance, pre-trial diet, and exercise control) were generally well controlled for, although only four studies screened for glucose tolerance. Only three studies were adequately powered [16, 37, 45]. 4 Discussion This is the first systematic review with meta-analysis evaluating the impact of the GI of a pre-exercise meal on endurance performance. The review demonstrates no sig- nificant ergogenic benefit of a LGI over a HGI pre-exercise meal. This was the case regardless of whether exogenous CHO was consumed during exercise. Metabolic responses including blood glucose and insulin secretion, FFA oxi- dation and RER were inconsistent between studies. Despite nydutS ES (95% CI) p value TTE (no CHO during exercise) ] 6 43 (- ) ] - - ) ] 8 56 - - ) Pooled effect (no CHO) - - ) Submax+TTE (no CHO during exercise) DeMarco ] 10 - - ) TTE (CHO during exercise) Reljic ] 34 9 - - - ) - - Favors HGI Fig. 4 Forest plot showing HGI vs. LGI pre-exercise meal effects on performance in time to exhaustion (TTE) trials without (n = 3; white squares) and with (n = 1; gray square) CHO ingestion during exercise. Studies are arranged according to GL differences between the HGI and LGI meals and size varies with subject number. Diamond represents the pooled effect from studies without CHO ingestion during exercise. CHO carbohydrate, CI confidence interval, Diff, difference, ES effect size, GL glycemic load, HGI high glycemic index, LGI low glycemic index Effect of Glycemic Index of a Pre-exercise Meal on Endurance Performance 123 the studies all having randomized cross-over designs, there was wide variability in research methodologies including the use of four main types of exercise performance tests, large differences in the timing and CHO content of pre- exercise meals, and a substantial range in the athletic cal- iber of participants between studies. Meta-regression did not identify any significant impact of these potential con- founding factors on performance, although the above inconsistencies and the relatively small number of studies within each exercise type may have limited the power to assess the impact of pre-exercise meal GI. The quality of the included articles was moderate and many studies were underpowered to assess the performance outcomes. The GI of the pre-exercise meal has been a relatively controversial aspect of the practical guidance provided to endurance athletes. Theoretically, a LGI pre-exercise meal may result in improved endurance performance as inges- tion is proposed to improve maintenance of blood glucose, reduce insulin secretion, facilitate the oxidation of free fatty acids, and spare muscle glycogen [50–52]. Despite these potential metabolic shifts induced by a LGI pre-ex- ercise meal, no significant benefit was observed from the meta-analysis conducted in this study across any of the four exercise testing protocols used. However, it should be noted that in none of the studies did the authors report a significant benefit of a HGI meal. All of the significant studies (n = 7) used LGI pre-exercise meals with exoge- nous CHO consumed during exercise in only one of these. Clearly, when CHO is ingested during exercise, this exogenous CHO is made available for oxidation and would support the pool of CHO available from body stores and decrease the risk of inadequate CHO availability during exercise [13]. This practice essentially negates a key ben- efit of a LGI pre-exercise meal. It should also be noted that there was a wide range of performance benefits reported in the seven significant studies (2.8–36.1 %) and only two used a TT design which is a more robust (lower coefficients of variation [53]) and relevant test of exercise performance. One of the limiting factors of the current literature on LGI pre-exercise meals and endurance performance is the relatively small number of studies within each exercise protocol used as well as the variability in the pre-exercise meal time, GL of meals, and training status of the partic- ipants. Pre-exercise meal time is an important factor, especially for LGI meals, as slower digestion may result in a delay in CHO availability for oxidation [54]. There was a wide range in pre-exercise meal time (30–210 min) across the studies, with some having as little as 30 min. This may have limited the capacity for CHO absorption and hence oxidation during exercise. All of the studies showing a non- significant benefit of a HGI meal had a pre-exercise meal timing of B2 h (excluding those where exogenous CHO was provided during exercise). In these studies, CHO from the HGI meal would have been available for oxidation earlier in exercise due to its faster absorption, whereas the CHO from the LGI meal was most likely less available earlier in exercise. Despite this, there were a number of a Coefficient: Standard error: p Ef fe ct s iz e (H ed ge s’ g) - - - - - - - b Coefficient: Standard error: p Ef fe ct s iz e (H ed ge s’ g) - - - - - Pre-exercise time (min) c Coefficient: - Standard error: p Ef fe ct s iz e (H ed ge s’ g) - - - - - - - VO2max (ml/kg/min) Fig. 5 Relationships between performance effect size and between- study variationsin: a HGI and LGI glycemic load difference; b pre- exercise meal timing; and c participant fitness. HGI high glycemic index, GL glycemic load, LGI low glycemic index, VO2max maximum oxygen uptake C. A. Burdon et al. 123 T a b le 3 E ff ec ts o f th e H G I an d L G I p re -e x er ci se m ea ls o n ex er ci se p er fo rm an ce an d m et ab o li c m ar k er s S tu d y P er fo rm an ce te st ty p e T es t m et ri c P er fo rm an ce o n H G Ia P er fo rm an ce o n L G Ia E ff ec t d ir ec ti o n fa v o rs (b y % d if fe re n ce )b S ig n ifi ca n t ef fe ct re p o rt ed ? M et ab o li c re sp o n se d u ri n g ex er ci se B en n et t et al . [3 8 ] T T M et er s 1 3 3 3 ± 1 0 0 1 3 2 8 ± 1 4 1 H G I (0 .4 ) N N o d if fe re n ce in g lu co se , in su li n , la ct at e, R E R , o r C H O o r fa t o x id at io n B u rk e et al . [3 3 ] S u b m ax ? T T M in u te s 1 5 .8 ± 0 .9 1 5 .9 ± 1 .5 H G I (0 .9 ) N N o d if fe re n ce in g lu co se , in su li n , F F A , R E R , o r C H O o x id at io n C h en et al . [2 2 ] S u b m ax ? T T M in u te s 5 2 .6 ± 5 .7 5 1 .2 ± 5 .7 L G I (2 .7 ) N R E R , la ct at e an d C H O o x id at io n lo w er , an d fa t o x id at io n h ig h er in L G I. N o d if fe re n ce in g lu co se , in su li n , o r F F A C h en et al . [3 4 ] S u b m ax ? T T M in u te s 9 1 .5 ± 6 .2 9 2 .4 ± 6 .8 H G I (1 .0 ) N N o d if fe re n ce in g lu co se , in su li n , C H O , o r fa t o x id at io n D eM ar co et al . [3 7 ] S u b m ax ? T T E M in u te s 2 .2 ± 1 .2 3 .4 ± 2 .3 L G I (3 6 .1 ) Y B et te r g lu co se m ai n te n an ce in L G I. R E R lo w er in L G I F eb b ra io an d S te w ar t [4 3 ] S u b m ax ? T T k J 2 5 0 ± 4 9 2 6 7 .0 ± 2 4 .5 L G I (6 .4 ) N N o d if fe re n ce in g lu co se , in su li n , la ct at e, R E R , o r C H O o x id at io n . F F A lo w er in H G I F eb b ra io et al . [4 2 ] S u b m ax ? T T k J 3 5 5 .0 ± 7 0 .7 3 3 2 .5 ± 1 0 6 .1 H G I (6 .5 ) N G lu co se lo w er in H G I 0 – 3 0 m in . F F A lo w er in H G I H u lt o n et al . [3 0 ] S u b m ax ? T T M in u te s 3 .6 ± 1 .1 3 .5 ± 0 .9 L G I (2 .7 ) N N o d if fe re n ce in g lu co se , in su li n , C H O o r fa t o x id at io n L it tl e et al . [3 2 ] T T M et er s 1 6 0 5 .5 ± 6 1 6 .2 1 6 2 7 .4 ± 5 3 6 .3 L G I (1 .4 ) N N o d if fe re n ce in g lu co se , C H O , o r fa t o x id at io n L it tl e et al . [3 9 ] T T M et er s 1 5 0 0 .0 ± 1 6 9 .5 1 5 1 0 .0 ± 1 7 6 .7 L G I (0 .7 ) N N o d if fe re n ce in g lu co se , in su li n , R E R , la ct at e, C H O , o r fa t o x id at io n M o o re et al . [4 0 ] T T M in u te s 9 5 .6 ± 6 .0 9 2 .5 ± 5 .2 L G I (3 .2 ) Y D u ri n g ex er ci se , R E R an d C H O o x id at io n h ig h er , an d fa t o x id at io n lo w er in L G I. A t en d o f ex er ci se , g lu co se h ig h er in L G I. N o d if fe re n ce in la ct at e M o o re et al . [4 1 ] T T M in u te s 9 6 .0 ± 7 .0 9 3 .0 ± 8 .0 L G I (3 .1 ) Y R E R an d C H O o x id at io n h ig h er , an d fa t o x id at io n lo w er in L G I. N o d if fe re n ce in g lu co se o r la ct at e R el ji c et al . [3 1 ] T T E M in u te s 7 3 .6 ± 1 2 .7 7 9 .7 ± 1 1 .7 L G I (7 .7 ) Y A ft er 6 0 m in , g lu co se h ig h er in L G I. N o d if fe re n ce in la ct at e S p ar k s et al . [4 4 ] S u b m ax ? T T k J 2 4 9 .0 ± 4 2 .4 2 5 3 .0 ± 2 8 .3 L G I (1 .6 ) N R E R an d C H O o x id at io n lo w er in L G I. A t 1 0 – 2 0 m in , g lu co se h ig h er in L G I. A t 2 0 an d 5 0 m in , F F A h ig h er in L G I T h o m as et al . [1 6 ] T T E M in u te s 9 7 .0 ± 2 9 .1 1 1 7 .0 ± 2 9 .1 L G I (1 7 .1 ) Y N o d if fe re n ce in g lu co se , in su li n , F F A , o r R E R . A t 0 – 1 5 m in an d 4 5 m in , la ct at e lo w er in L G I. T h o m as et al . [4 8 ] T T E M in u te s 9 4 .0 ± 2 6 .9 9 0 .0 ± 1 9 .6 H G I (4 .3 ) N N o d if fe re n ce in g lu co se , in su li n , F F A , la ct at e, o r R E R . A t en d o f ex er ci se , g lu co se h ig h er in L G I, an d R E R lo w er in L G I W o n g et al . [4 5 ] S u b m ax ? T T M in u te s 1 0 1 .5 ± 5 .9 9 8 .7 ± 5 .7 L G I (2 .8 ) Y A t 5 – 1 0 k m , R E R an d C H O o x id at io n lo w er in L G I. A t 5 – 1 5 k m , fa t o x id at io n h ig h er in L G I. A t 1 0 k m , g lu co se h ig h er in L G I. A t 1 0 – 2 1 k m , g ly ce ro l h ig h er in L G I. A t en d o f ex er ci se , F F A h ig h er in L G I. N o d if fe re n ce in in su li n , la ct at e W o n g et al . [4 7 ] S u b m ax ? T T M in u te s 9 1 .1 ± 6 .0 9 1 .8 ± 6 .6 HG I (0 .8 ) N N o d if fe re n ce in g lu co se , in su li n , la ct at e, F F A , g ly ce ro l, C H O , o r fa t o x id at io n W u an d W il li am s [4 9 ] T T E M in u te s 1 0 1 .4 ± 1 4 .7 1 0 8 .8 ± 1 1 .6 L G I (6 .8 ) Y A t 0 – 3 0 m in , g lu co se h ig h er in L G I. A t 4 5 m in , g ly ce ro l h ig h er in L G I. A t 0 – 9 0 m in , fa t o x id at io n h ig h er , an d C H O o x id at io n lo w er in L G I. F F A h ig h er an d R E R lo w er in L G I th ro u g h o u t. N o d if fe re n ce in la ct at e C H O ca rb o h y d ra te , F F A fr ee fa tt y ac id , H G I h ig h g ly ce m ic in d ex , L G I lo w g ly ce m ic in d ex , N n o , R E R R es p ir at o ry ex ch an g e ra ti o , S u b m a x su b m ax im al ex er ci se , T T ti m e tr ia l, T T E ti m e to ex h au st io n , Y y es a V al u es ar e m ea n ± S D b P er ce n t d if fe re n ce ca lc u la te d as th e im p ro v em en t o f o n e tr ia l o v er th e o th er , e. g ., (L G I- H G I) /L G I 9 1 0 0 , h o w ev er fo r th e p u rp o se o f th e w ei g h te d m ea n d if fe re n ce , th e sa m e eq u at io n w as u se d Effect of Glycemic Index of a Pre-exercise Meal on Endurance Performance 123 studies (n = 6) where the LGI meal (without exogenous CHO consumption) was reported to have a significant effect. In four of these studies, the meal was provided\1 h before exercise and it is possible that despite the short pre- exercise meal time, at least some CHO from the LGI meal was still available at the later stages of exercise to support CHO oxidation when endogenous stores were low. Current sports nutrition guidelines recommend con- sumption of the pre-exercise meal 1–4 h prior [1]. Time- frames outside of these recommendations were used in seven of the 19 studies. At the time when most of the included studies were conducted, there was concern regarding the potential for a HGI meal to cause a nadir in blood glucose close to the commencement of exercise and so studies were often purposely designed to investigate this effect. This explains why a number (n = 7) of the studies in this review were designed with a\1-h pre-exercise meal time despite the risk that for the LGI condition, this may have compromised CHO availability during exercise. Despite concern regarding the potential for hypoglycemia after a HGI pre-exercise meal, none of the studies reported any participant experiencing symptoms of hypo- glycemia although some studies did report a few partici- pants experiencing blood glucose concentrations below 3.5 mmol/L. Another parameter which varied widely across the studies was the GL. As the studies all included a similar dose of CHO in both arms, it was not possible to quanti- tatively examine the within-study impact of GL. Qualita- tive evaluation of the forest plots with studies arranged from lowest to highest within-study GL differences does not support any effect of meal GL. The dose of CHO in a pre-exercise meal recommended by current sports nutrition guidelines is 1–4 g/kg body mass. All but one of the included studies used this dose, although all of the studies were in the lower half of this range (B2 g/kg). At a higher pre-exercise CHO dose, there may be a greater effect of the GL, although this has not yet been investigated. Table 4 Methodological quality of included studiesa Study Reporting EV Bias Confounding Power Study score (max 21) 1 2 3 4 5 6 7 8 9 10 11 12 13 14b 15 16 17 18 19 Bennett et al. [38] Y Y Y Y Y Y N Y Y N Y Y Y U Y Y N Y Y N 15 Burke et al. [33] Y Y N Y Y Y N N Y N Y N Y Y Y Y N Y Y N 14 Chen et al. [22] Y Y N Y Y Y N N Y Y Y Y Y P Y Y N Y Y N 15 Chen et al. [34] Y Y Y Y Y Y N N Y N N N Y P Y Y Y Y N N 13 DeMarco et al. [37] Y Y Y Y Y Y N N Y N Y N Y U Y Y Y Y Y Y 15 Febbraio and Stewart [43] Y Y N Y Y Y N N Y N N N Y U Y Y N Y Y N 11 Febbraio et al. [42] Y Y N Y Y Y N N Y N N N Y U Y Y N Y Y N 13 Houlton et al. [30] Y Y N Y Y Y Y N U N Y N Y P Y Y N Y Y N 11 Little et al. [32] Y Y N Y Y Y Y Y Y N Y Y Y P Y Y N Y Y N 16 Little et al. [39] Y Y N Y Y Y N N Y N Y N Y P Y Y N Y Y N 13 Moore et al. [40] Y Y N Y Y Y N Y Y Y Y Y Y Y Y Y N Y Y N 17 Moore et al. [41] Y Y N Y Y Y Y Y Y N Y N Y P Y Y N Y Y N 15 Reljic et al. [31] N Y Y Y Y Y N N U N N Y Y U Y Y N Y Y N 11 Sparks et al. [44] Y Y N Y Y Y N N Y N N N Y P Y Y N Y Y N 12 Thomas et al. [16] Y Y N Y Y Y N N Y Y Y N Y U Y Y N Y Y Y 14 Thomas et al. [48] Y Y N Y Y Y N N Y Y Y N Y U Y Y N Y Y N 13 Wong et al. [45] Y Y Y Y Y Y N N Y N Y Y Y P Y Y Y Y Y Y 17 Wong et al. [47] Y Y Y Y Y Y N N Y N N N Y P Y Y Y Y Y N 14 Wu and Williams [49] Y Y N Y Y Y N N Y N N N Y U Y Y N Y Y N 11 Item score (max 19) 18 19 6 19 19 19 3 4 17 4 12 6 19 6.5 19 19 4 19 18 3 1 hypothesis stated, 2 main outcomes, 3 participant description, 4 intervention described, 5 main findings described, 6 variability estimates, 7 adverse events reported, 8 actual p value reported, 9 representative subjects, 10 subject blind to food, 11 subject blind to performance, 12 researcher blinded, 13 statistical tests, 14 compliance, 15 accurate measures, 16 randomized to groups, 17 glucose tolerance screening, 18 24 h diet control, 19 24 h exercise control, EV external validity, Max maximum, N no, P partial, U unable to determine, Y yes a For all items except that assessing compliance, ‘‘Y’’ is given a score of one and ‘‘N’’ or ‘‘U’’ are given a score of zero b Item 14 on compliance is given a maximum score of two, with ‘‘Y’’ scored as two, ‘‘P’’ as one, and ‘‘U’’ as zero C. A. Burdon et al. 123 Participant fitness is another variable that may influence performance outcomes. Performance coefficients of varia- tion in participants of higher athletic caliber are often smaller, providing a greater chance to observe significant effects [53]. Fitter participants also have a greater capacity to oxidize fat, and, thus, their reliance on CHO oxidation during sub-maximal exercise may be lower [46]. The type of exercise test is also relevant to measuring performance. In this review, only two studies used well trained partici- pants, which limited the generalizability of the results to elite athletes. However, elite endurance athletes are also likely to use exogenous CHO during exercise so this is another key reason why there could be limited applicability of a LGI pre-exercise meal. Lack of consistency of these factors limits the capacity to draw firm conclusions, although meta-regression analysis failed to identify any of these factors as having a significant impact on the overall outcomes. Consistent with the above limitations, the metabolic responses reported across the studies were also conflicting. Half of the 14 studies where exogenous CHO was not consumed reported no difference in blood glucose con- centration between the LGI and the HGI meals. Ten of the 12 studies reporting on blood lactate also showed no dif-ference between meals. Many of the studies (but not all) reported lower free fatty acid (six of nine), higher CHO oxidation rate (five out of 11), and a higher RER (six of 12) with the HGI pre-exercise meal, which would be antici- pated on theoretical grounds [50–52]. Lack of control of pre-exercise diet and exercise regimens as well as between- study variability in participant fitness and GL may have influenced the metabolic results. It is also notable that all except one of the pre-exercise meals had mixed macronu- trient composition rather than being CHO alone. Other nutrients, particularly protein, are known to influence post- prandial insulin release [55]. Although the meals were matched within each study, substantial variation in meal composition existed across studies, which likely played a role in the different metabolic responses observed in this review. Given that most elite endurance athletes consume exogenous CHO during exercise and competitions provide aid stations to support this, the real-world application of a LGI pre-event meal in competitive sport may be limited. However, our analysis suggests there may be some situa- tions in which a LGI meal could be beneficial. These sit- uations include prolonged exercise where there is limited opportunity for exogenous CHO ingestion, such as intense and sustained physical activity during military operations. There may also be an application for athletes with a dis- ability in wheelchair or hand-cycling endurance events as although there are sufficient aid stations to provide exogenous CHO, it may be logistically difficult for the athletes to take their hands off the wheel or bike wheel crank (unless they are going downhill). Storing drinks containing CHO can also be difficult in the bike/chair set- up and fluid requirements are substantially lower in those with spinal cord injury as they do not sweat below the level of lesion [56]. There may also be some application for individuals who are unable to tolerate exogenous CHO consumption at the high levels required for performance optimization. Over the past 10 years there has been interest in maximal CHO oxidation rates during endurance exercise and in strategies to enhance CHO absorption from the gut [57]. Amounts of up to 90 g of CHO per hour can be successfully fed using 2:1 glucose to fructose ratios, and the subsequent gain in CHO oxidation rate may be essential to winning perfor- mance for top athletes during endurance events [58]. It can be difficult for some athletes to consume CHO at these rates due to gastrointestinal upset [59], although CHO tolerance has been shown to improve with regular CHO ingestion during exercise [60]. LGI pre-exercise meals may be useful in athletes whose CHO tolerance remains low. This potential application of a LGI meal warrants further investigation. This review has a number of strengths in that it was systematic and also included meta-analysis with sub- analysis conducted for studies where CHO was ingested during exercise, as is typical for endurance events. Meta- regression was also used to investigate the influence of potential effect modifiers: the GL, pre-exercise meal timing, and participant fitness. Weaknesses include the quality of the included studies, which was mixed due to inadequate description of the participants and any adverse events, lack of participant blinding, inadequate description/reporting of the diet control in the 24 h prior to the exercise performance tests, and lack of statistical power in most of the studies. In many of the studies, the meals were fed\2 h prior to exercise and it was likely that much of the LGI CHO remained undigested and therefore unavailable for oxidation. This limited the capacity to fully evaluate the effectiveness of the LGI meal. Future research in this area would benefit from a focus on situations where it may be more difficult for participants to consume CHO during exercise such as extended military operations and endurance events for athletes with a dis- ability (wheelchair marathons/hand cycling) where com- petitors may find it logistically difficult to access CHO during the event. In these situations, slowly digested LGI CHO may support CHO oxidation later in the event. Consumption of a LGI pre-event CHO meal may also be useful for elite athletes with high rates of CHO oxidation who experience gastrointestinal distress when consuming higher amounts of exogenous CHO during the event. Effect of Glycemic Index of a Pre-exercise Meal on Endurance Performance 123 5 Conclusion In conclusion, this systematic review and meta-analysis does not support a significant benefit of a LGI over a HGI meal for endurance exercise performance. The metabolic responses to these meals were also inconsistent. Given that exogenous CHO consumption is common practice for athletes during endurance events, it would seem that LGI pre-event meals have limited benefit in competitive endurance sports. 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