HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Free All Versions of this Article: 103/3/995    most recent 00018.2007v1 Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Timmons, B. W. Articles by Riddell, M. C. Search for Related Content PubMed PubMed Citation Articles by Timmons, B. W. Articles by Riddell, M. C.

Energy substrate utilization during prolonged exercise with and without carbohydrate intake in preadolescent and adolescent girls

Brian W. Timmons,¹ Oded Bar-Or,^1, and Michael C. Riddell²

¹Children's Exercise and Nutrition Centre, McMaster University, Hamilton, Ontario; and ²School of Kinesiology and Health Science, Faculty of Science and Engineering, York University, Toronto, Ontario, Canada

Submitted 4 January 2007 ; accepted in final form 28 June 2007

	ABSTRACT

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Little information is available on energy metabolism during exercise in girls, particularly the contribution of exogenous carbohydrate (CHO_exo). The purpose of this study was to determine substrate utilization during exercise with and without CHO_exo intake in healthy girls. Twelve-yr-old preadolescent (YG; n = 12) and 14-yr-old adolescent (OG; n = 10) girls consumed flavored water (WT) or ¹³C-enriched 6% CHO (CT) while cycling for 60 min at 70% maximal aerobic power (O_2max). Substrate utilization was calculated for the final 15 min of exercise. CHO_exo decreased fat oxidation by 50% in YG but not in OG (P < 0.001) and decreased endogenous CHO oxidation by 15% in OG but not in YG (P = 0.006). Endogenous CHO oxidation was lower in YG than in OG regardless of trial (P 0.01), whereas fat oxidation was higher in YG only during WT (P < 0.001). CHO_exo oxidation rate was similar between YG and OG (7.1 ± 0.5 and 6.8 ± 0.4 mg·kg^–1·min^–1, respectively, P = 0.67), contributing 19% to total energy expenditure. Serum estradiol levels in all girls correlated with fat (r = –0.50 to –0.59, P = 0.03 to 0.005) and endogenous CHO oxidation (r = 0.50 to 0.63, P = 0.03 to 0.005) but not with CHO_exo oxidation (r = –0.09, P = 0.71). We conclude that CHO_exo influences endogenous substrate utilization in an age-dependent manner in healthy girls but that total CHO_exo oxidation during exercise is not different between YG and OG. Our results also point to potential sex-related differences in energy substrate utilization even during childhood.

children; cycling; energy metabolism; stable isotope tracers

To further explore the impact of growth and development on energy metabolism during exercise, we have employed ¹³C stable isotope methodology in healthy boys and in boys with insulin-dependent diabetes mellitus (22–24, 33, 34). This technique, which provides quantification of exogenous carbohydrate (CHO_exo) and CHO_endo oxidation, is safe and noninvasive and therefore appealing for use in children. Using this approach, it has been found that, compared with adult men, pre- and early-pubertal boys exhibit a higher rate of CHO_exo oxidation (33) and that advanced pubertal status, independently of chronological age, reduces the contribution of CHO_exo oxidation to total energy expenditure (34). These findings were somewhat surprising because a common view in pediatric exercise physiology is that children possess an underdeveloped glycolytic capacity and are, therefore, "immature" in their ability to oxidize glucose in skeletal muscle (1). Despite the new information gained from our studies with ¹³C-labeled CHO, a significant limitation of these studies was that they were exclusively conducted with male participants. Only a few studies have been conducted that examine CHO_exo oxidation rates during exercise in adult females, but none with young girls. The available adult studies report a similar (13, 36) or slightly higher (25) contribution of CHO_exo oxidation to total energy expenditure (EE) in women compared with men. Whether the presence of sex steroids influences the reliance on CHO_exo oxidation during exercise remains unclear. On the basis of the above adult studies, it has been suggested that, compared with men, women may derive at least as much benefit from consuming CHO_exo during athletic competition (36). Whether this possibility also holds true in young girls is not known, but we have shown that CHO_exo supplementation improves endurance performance in boys (24). If similar age-related differences in CHO_exo oxidation exist in girls as they do in boys (34), this information would be important for age- and sex-specific dietary recommendations for sport and athletic performance.

The purpose of this study was therefore to characterize substrate utilization during exercise performed with and without CHO_exo in healthy preadolescent and adolescent girls. To achieve this objective, we employed an established protocol of endurance exercise and ¹³C stable isotope methods. On the basis of our previous findings of higher fat and CHO_exo oxidation relative to body weight in boys compared with men (33) and in younger compared with older boys (34), we hypothesized that the contribution from fat and CHO_exo oxidation to total energy yield would also be higher in 12-yr-old preadolescent girls (YG) compared with 14-yr-old adolescent girls (OG).

	METHODS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Subjects.   Twenty-two girls participated in this study approved by the McMaster University Research Ethics Review Board. All girls were healthy, active, and not taking medication, including oral contraceptives. All girls in the OG group (n = 10) experienced regular menstrual cycles, whereas only 4 of the 12 girls in the YG group had experienced their first menstrual period but none experienced regular cycles. After the purpose, procedures, and risks of the study were explained, the girls agreed verbally to participate, and their parent then signed a written informed consent. Pubertal status of each girl was self-assessed and based on breast development according to Tanner (31). Self-assessment of pubertal status has been shown to be valid and reproducible among girls (18). To provide a more objective indication of each girl's pubertal status, we also determined their serum estradiol level (see Hormone and metabolite analysis). Table 1 provides the subjects' characteristics.

Experimental sessions.   Each subject completed two experimental trials a minimum of 4 days and a maximum of 4 wk apart. Trials were conducted in a double-blind and counterbalanced manner. All girls in the OG group were tested in the early follicular phase of their menstrual cycle. Because of the sporadic nature of menstruation in four of the girls in the YG group, we did not attempt to test these girls at a particular time. Nutrient intake and physical activity over the 2 days before both experimental trials were standardized by having the girls repeat the same nutrient intake and physical activity. Strenuous exercise was also avoided for these 2 days. Corn products or food derived from plants with the C₄ photosynthetic cycle was avoided to reduce background enrichment of expired CO₂ from naturally derived ¹³C (29). Subjects arrived to the laboratory at the same time on the day of testing in a 10-h fasted state. An indwelling venous catheter (Becton Dickinson) was placed in either an arm or a hand, followed by 10 min of supine rest before the preexercise blood sample was drawn (40 min before the start of exercise). Subjects then consumed a small breakfast with their first drink (12 ml/kg body mass) to standardize preexercise nutrition. This snack, consumed within 3–5 min, consisted of one slice of toast with sugar-free jam (90 kcal) for girls in the YG group and twice this for the OG group; this approach is consistent with our previously published work (33, 34). Volumes of 4 ml/kg body mass were subsequently consumed at 15-min intervals throughout exercise. This drinking schedule is similar to that used in our previous studies (33, 34). In the CHO trial (CT), subjects consumed 28 ml/kg body mass of a 6% CHO-electrolyte solution (4% sucrose, 2% glucose, 18 mM Na⁺, 3 mM K⁺), and in the water trial (WT), an identical volume of flavored water (identical in flavor, sweetness, and electrolyte concentration, but without CHO) was consumed. Both beverages were prepared in powder form by the Gatorade Sports Science Institute (Barrington, IL). The CHO drink was artificially enriched with uniformly labeled [¹³C]glucose to an isotopic composition of +10.0 change per 1,000 difference vs. the ¹³C/¹²C ratio from the international standard ¹³C Pee Dee Belemnitella-1 (+10.0[-¹³C]PDB-1). This value was determined using gas chromatography-mass spectrometry. Previous work by us (23, 24) and others (20) shows that the use of [¹³C]glucose rather than ¹³C-labeled glucose/sucrose as a tracer is quite reasonable, given the similar oxidation rates of these carbohydrates during exercise.

Forty minutes after the resting blood sample (35 min after the snack), subjects began cycling at a power output estimated to be 70% of their predetermined O_2max. The exercise duration (60 min) and intensity used in this study were chosen to maintain consistency with our previously published papers (33, 34). The pedaling rate remained constant at 60 rpm throughout exercise, which consisted of two 30-min bouts separated by a 5- to 7-min rest period. Additional expired gas samples were collected throughout the exercise bout to ensure the proper work intensity, with the power output adjusted accordingly. The actual O₂ consumption (O₂) during exercise was maintained at 67 ± 1% O_2max. Expired gas was collected in the second 30-min bout of exercise between minutes 12 and 17 and for the last 5 min; these values were then averaged and used for substrate calculations for each trial. Postexercise blood samples were collected at 60 min of exercise while subjects remained seated on the cycle ergometer.

Substrate utilization.   Oxidation rates of fat and total CHO (CHO_total) were calculated according to the following equations (21):

(1)

(2)

where CO₂ is CO₂ production. The energy provided from fat and CHO oxidation was calculated from their energy potentials (9.75 kcal/g and 3.87 kcal/g, respectively). To measure the ratio of ¹³C/¹²C in expired CO₂, a 20-ml syringe was used to draw a sample of the expired gas directly from the tube connecting the subject's mouthpiece to the metabolic cart during the last expired breath collection. Duplicate samples (10 ml) were emptied from the syringe into Vacutainer tubes (Becton Dickinson) and subsequently analyzed for the ratio of ¹³C/¹²C (BreathMat Plus, Finnigan MAT). CHO_exo oxidation was calculated according to the equation modified from Mosora et al. (19):

(3)

where CO₂ (l/min) is in STPD, R_exp is the isotopic composition of expired CO₂ during CT, R_ref is the isotopic composition of expired CO₂ during WT at the corresponding time point, R_exo is the isotopic composition of the CHO_exo, and k (0.7426 l/g) is the volume of CO₂ produced by the complete oxidation of 1 g of glucose. CHO_endo oxidation was calculated by subtraction.

Hormone and metabolite analysis.   Whole blood collected at rest was allowed to clot and then centrifuged at 2,000 g for 10 min. Serum was stored at –70°C until analyzed in duplicate for estradiol, which was used as an objective indication of pubertal status, using a commercially available RIA kit (cat. no. TKE21, Diagnostic Products). Growth hormone (GH) was measured in pre- and postexercise serum using a commercially available RIA kit (cat. no. KGHD1, Diagnostic Products). In our hands, the intra- and interassay CVs, respectively, are 8 and 8% for estradiol and 5 and 12% for GH. Whole blood collected at rest and at 60 min of exercise was treated with EGTA and reduced glutathione and centrifuged at 2,000 g for 10 min, and the plasma was stored at –70°C until analyzed for epinephrine (Epi) and norepinephrine (NE). Plasma catecholamines were analyzed by high-performance liquid chromatography with electrochemical detection as previously described (16). The intraclass correlation of this procedure is 0.96, representing very high reliability, and the extraction efficiency from plasma ranges between 80 and 85%. Whole blood collected before and immediately after exercise was also treated with EDTA and centrifuged at 2,000 g for 10 min. The plasma was stored at –50°C until analyzed for glucose and lactate concentrations enzymatically (2300L STAT, Yellow Springs Instruments). The intra- and interassay coefficients of variation for this assay were <1.5%.

Statistical analyses.   Age differences in physical and fitness characteristics and CHO_exo oxidation-related variables were tested by independent t-tests. Substrate utilization data were submitted to group x trial mixed-factorial ANOVAs. Metabolite and hormone data were submitted to group x trial x time mixed-factorial ANOVAs. Where appropriate, a Tukey's post hoc test was used to determine significance among means. Statistica 5.0 (StatSoft, Tulsa, OK) was used for all statistical comparisons. Pearson correlations between substrate utilization, expressed as a percentage of total EE, and estradiol levels were also performed using GraphPad Prism 4.03 (GraphPad Software, San Diego, CA). The threshold for statistical significance was set at P 0.05, and data are presented as means ± SE, unless stated otherwise.

	RESULTS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Hormones and metabolites (Tables 1 and 2).   Serum estradiol levels (Table 1) were lower in YG than in OG (P < 0.05). Regardless of trial, GH, Epi, and NE increased in response to exercise (time effect, P < 0.05), but this response was not different between groups (group x trial x time effect, P 0.17). The GH response was greater during WT than CT (trial x time effect, P < 0.05). There were no intergroup differences in preexercise glucose in either trial (P 0.60). There was a trend for a group x trial x time interaction (P = 0.07) for lactate, with values higher in OG than YG during WT but not during CT.

View larger version (8K): [in this window] [in a new window]   Fig. 1. Respiratory exchange ratio (RER) during last 15 min of exercise in water (WT) and carbohydrate trials (CT) in 12-yr-old preadolescent (YG) and 14-yr-old adolescent girls (OG). Values are means ± SE. Main effects for group (P < 0.05) and trial (P < 0.05), as well as a group by trial interaction (P < 0.05), were found. *Significantly different from YG in same trial, P < 0.05. Significantly different from WT in same group, P < 0.05.

View larger version (13K): [in this window] [in a new window]   Fig. 2. Percent of energy expenditure derived from substrate during last 15 min of exercise in 12-yr-old preadolescent (A) and 14-yr-old adolescent girls (B). Hatched bars, fat oxidation; solid bars, endogenous carbohydrate (CHOendo) oxidation; open bars, exogenous carbohydrate (CHOexo) oxidation. Significantly different from WT in same group, P < 0.05.

	DISCUSSION

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

A more than twofold higher rate of fat oxidation during exercise performed without CHO_exo in YG compared with their OG counterparts (Table 3) is consistent with our previous findings comparing 12- and 14-yr-old boys (34). Thus, compared with older adolescents, younger children have considerably higher rates of fat oxidation during exercise. Higher fat oxidation rates are also observed in women compared with men (32), and acute estrogen supplementation in men increases fat oxidation toward a female profile (10), indicating that an elevated estrogen level may alter the balance of fat and CHO_endo oxidation during exercise. However, our results do not entirely support a role for estrogen because the girls in YG experienced the highest fat oxidation rates despite having 50% lower serum estradiol concentrations, and, in all girls, the degree of fat oxidation was inversely related to estradiol concentration. It is clear, therefore, that factors other than estrogen promote high rates of fat oxidation in young girls. Increases in serum GH during exercise, for example, are smaller in women than in men (37), and GH is thought to induce lipolysis and mobilization of fatty acids during exercise (4). In the present study, the GH response to exercise was similar between the YG and OG (Table 2), suggesting that this lipolytic hormone did not play a role in our findings. Catecholamines can also influence glycogenolysis and fatty acid mobilization during exercise, and there is evidence for sex differences in these hormone responses to exercise in adults (5), but there were no differences between groups in either epinephrine or norepinephrine responses in this study (Table 2). Given the lack of differences in catecholamines and GH, it is possible that the greater reliance on fat oxidation during exercise in YG may be due to differences in other lipolytic hormones, such as glucocorticoids, or perhaps differences in enzyme activity within the contracting muscle. These potential differences between YG and OG require further consideration.

In an early study (7), phosphofructokinase, the rate-limiting enzyme in glycolysis, was reported to be lower in children compared with adults. Although these data were derived from only five boys at rest, and age-related variation in this enzyme has not been substantiated by subsequent studies (2, 6, 11), the work of Eriksson (7) led to a commonly held belief that children possess a relatively underdeveloped glycolytic system (1). Other studies have measured lactate dehydrogenase in muscle and found lower activity in children compared with adults (12), higher activity in 13-yr-old children compared with younger children (6 yr old) or older adolescents (17 yr old) (2), or similar activity between adolescents and adults (11). Given the clear discrepancies in muscle enzyme data and because the 12-yr-old girls tested in this study demonstrated a similar capacity to utilize CHO_exo compared with the 14-yr-old girls, we do not believe that children possess an underdeveloped glycolytic capacity. In previous studies, we have found the rate of CHO_exo oxidation to be, in fact, higher in 9- to 10-yr-old boys compared with adult male (33) and compared with 12- vs. 14-yr-old boys (34), further supporting our notion that the ability to utilize glucose in skeletal muscle is not impaired in young children. Whether enzyme activities of the tricarboxylic acid cycle or -oxidation are higher in the younger children is not clear, but these enzymes have been found to be comparable (7, 12) or even higher (2, 11) in children than those reported for adults.

The most novel finding in this study is that the contribution of CHO_exo to total EE and the balance between exogenous and endogenous CHO utilization during exercise were not different between YG and OG. In contrast, we recently reported that the reliance on CHO_exo oxidation was higher in 12-yr-old compared with 14-yr-old boys (34), indicating a greater relative conservation of glycogen in the younger boys. It has been reported in boys that both resting muscle glycogen content and the rate of muscle glycogenolysis during exercise performed without CHO_exo increase with testicular volume, a marker of pubertal status, during childhood (8). Indeed, our male data support this finding insofar as the ratio of CHO_exo to CHO_endo oxidation was also lower in less mature compared with more mature boys who were all at the same chronological age (34). The fact that there was only a small, albeit statistically significant, gap in pubertal status between the girls in the YG and OG groups in the present study (Tanner 3 vs. Tanner 4, respectively) may explain, in part, the lack of difference between groups in the reliance on CHO_exo and the ratio of CHO_exo to CHO_endo oxidation. Consistent with this possibility is the finding that lactate levels were generally similar between the groups of girls during the CHO trial, as the lactate response to exercise tends to be greater in more mature individuals (1). In addition, these observations suggest that the presence of estrogen does not influence CHO_exo oxidation, at least in youth. Therefore, it will be important to further elucidate the impact of pubertal status, rather than age per se, on the balance of exogenous and endogenous sources of fuel during exercise in girls.

Given the direct relationship between resting muscle glycogen content and its utilization during exercise observed in adults (3), we speculated that age-related differences in the reliance on CHO_endo oxidation previously observed in boys (34) is due to lower initial muscle glycogen levels rather than a reduced capacity to utilize glycogen. We therefore suggest that a similar phenomenon occurs in girls, as indicated by the present results. Consequently, children may compensate for reduced muscle glycogenolysis by increasing their reliance on extramuscular sources of fuel (e.g., adipose-derived free fatty acids, liver gluconeogenesis, or CHO_exo when available). Given the lack of age differences in CHO_exo oxidation among the girls in this study, it remains possible that regulation of extramuscular fuel mobilization during exercise is different between boys and girls. Additional evidence that regulation of fuel mobilization may be different in boys and girls is based on our finding that CHO_exo reduced fat oxidation in YG but not in OG, whereas the effect was similar in young compared with older boys (34). Additional studies using minimally invasive stable isotope methodology should help to clarify these points.

In summary, CHO_exo intake reduced fat oxidation in YG but did not alter fat oxidation in OG. Despite these effects on fat oxidation, the contribution of CHO_exo to total EE was not different between the YG and OG groups. These findings are in contrast to previous studies with boys in which the reliance on CHO_exo during exercise was shown to be particularly sensitive to pubertal status, and there were no age-related differences in endogenous fuel sparing with CHO_exo intake. These novel findings highlight the notion that sex differences exist in substrate utilization during exercise even in childhood. In addition, our data do not support the idea of underdeveloped glycolytic flux in children but rather an underdeveloped depot of intramuscular fuels.

	GRANTS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
The financial support of the Gatorade Sports Science Institute (GSSI) is gratefully acknowledged. B. W. Timmons is supported by a Canadian Institutes of Health Research Industry-partnered (GSSI) Postdoctoral Fellowship. M. C. Riddell is supported by an operating grant from the Natural Sciences and Engineering Research Council of Canada (Grant 261306).

	ACKNOWLEDGMENTS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
We thank Melanie De Jonge, Marta Kubacki, Raymond Trott, Jae-Hunn Lee, Mazen Hamadeh, and Amy Mark for assistance with this experiment and Melanie Wolfe for technical assistance in measuring ¹³C/¹²C of expired CO₂ gas samples. The extraordinary effort and time of our subjects are gratefully acknowledged.

	FOOTNOTES

 

Address for reprint requests and other correspondence: M. C. Riddell, School of Kinesiology and Health Science, York Univ., 4700 Keele St., Toronto, Ontario, Canada M3J 1P3 (e-mail: mriddell{at}yorku.ca)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Deceased December 2005.

	REFERENCES

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 

1. Bar-Or O, Rowland TW. Pediatric Exercise Medicine: From Physiologic Principles to Health Care Applications. Champaign, IL: Human Kinetics, 2004.
2. Berg A, Kim SS, Keul J. Skeletal muscle enzyme activities in healthy young subjects. Int J Sports Med 7: 236–239, 1986.[Web of Science][Medline]
3. Bergstrom J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical performance. Acta Physiol Scand 71: 140–150, 1967.[Web of Science][Medline]
4. Brandou F, Aloulou I, Razimbaud A, Fedou C, Mercier J, Brun JF. Lower ability to oxidize lipids in adult patients with growth hormone (GH) deficiency: reversal under GH treatment. Clin Endocrinol (Oxf) 65: 423–428, 2006.[CrossRef][Medline]
5. Braun B, Horton T. Endocrine regulation of exercise substrate utilization in women compared to men. Exerc Sport Sci Rev 29: 149–154, 2001.[CrossRef][Medline]
6. Colling-Saltin AS. Some quantitative biochemical evaluations of developing skeletal muscles in the human foetus. J Neurol Sci 39: 187–198, 1978.[CrossRef][Web of Science][Medline]
7. Eriksson BO. Physical training, oxygen supply and muscle metabolism in 11–13-year old boys. Acta Physiol Scand Suppl 384: 1–48, 1972.[Medline]
8. Eriksson BO, Karlsson J, Saltin B. Muscle metabolites during exercise in pubertal boys. Acta Paediatr Scand Suppl 217: 154–157, 1971.[Medline]
9. Foricher JM, Ville N, Gratas-Delamarche A, Delamarche P. Effects of submaximal intensity cycle ergometry for one hour on substrate utilisation in trained prepubertal boys versus trained adults. J Sports Med Phys Fitness 43: 36–43, 2003.[Web of Science][Medline]
10. Hamadeh MJ, Devries MC, Tarnopolsky MA. Estrogen supplementation reduces whole body leucine and carbohydrate oxidation and increases lipid oxidation in men during endurance exercise. J Clin Endocrinol Metab 90: 3592–3599, 2005.[Abstract/Free Full Text]
11. Haralambie G. Enzyme activities in skeletal muscle of 13–15 years old adolescents. Bull Eur Physiopath Respir 18: 65–74, 1982.[Web of Science][Medline]
12. Kaczor JJ, Ziolkowski W, Popinigis J, Tarnopolsky MA. Anaerobic and aerobic enzyme activities in human skeletal muscle from children and adults. Pediatr Res 57: 331–335, 2005.[CrossRef][Web of Science][Medline]
13. M'Kaouar H, Peronnet F, Massicotte D, Lavoie C. Gender difference in the metabolic response to prolonged exercise with [¹³C]glucose ingestion. Eur J Appl Physiol 92: 462–469, 2004.[Web of Science][Medline]
14. Macek M, Vavra J. Cardiopulmonary and metabolic changes during exercise in children 6–14 years old. J Appl Physiol 30: 202–204, 1971.
15. Mahon AD, Duncan GE, Howe CA, Del Corral P. Blood lactate and perceived exertion relative to ventilatory threshold: boys versus men. Med Sci Sports Exerc 29: 1332–1337, 1997.
16. Marra S, Burnett M, Hoffman-Goetz L. Intravenous catecholamine administration affects mouse intestinal lymphocyte number and apoptosis. J Neuroimmunol 158: 76–85, 2005.[CrossRef][Web of Science][Medline]
17. Martinez LR, Haymes EM. Substrate utilization during treadmill running in prepubertal girls and women. Med Sci Sports Exerc 24: 975–983, 1992.
18. Matsudo SMM, Matsudo VKR. Self-assessment and physician assessment of sexual maturation in Brazilian boys and girls: Concordance and reproducibility. Am J Hum Biol 6: 451–455, 1994.[CrossRef][Web of Science]
19. Mosora F, Lefebvre P, Pirnay F, Lacroix M, Luyckx A, Duchesne J. Quantitative evaluation of the oxidation of an exogenous glucose load using naturally labeled ¹³C-glucose. Metabolism 25: 1575–1582, 1976.[CrossRef][Web of Science][Medline]
20. Peronnet F, Adopo E, Massicotte D, Hillaire-Marcel C. Exogenous substrate oxidation during exercise: studies using isotopic labelling. Int J Sports Med 13, Suppl 1: S123–S125, 1992.[Web of Science][Medline]
21. Peronnet F, Massicotte D. Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16: 23–29, 1991.[Web of Science][Medline]
22. Riddell MC, Bar-Or O, Hollidge-Horvat M, Schwarcz HP, Heigenhauser GJ. Glucose ingestion and substrate utilization during exercise in boys with IDDM. J Appl Physiol 88: 1239–1246, 2000.[Abstract/Free Full Text]
23. Riddell MC, Bar-Or O, Schwarcz HP, Heigenhauser GJ. Substrate utilization in boys during exercise with [¹³C]-glucose ingestion. Eur J Appl Physiol 83: 441–448, 2000.[CrossRef][Web of Science][Medline]
24. Riddell MC, Bar-Or O, Wilk B, Parolin ML, 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.[Abstract/Free Full Text]
25. Riddell MC, Partington SL, Stupka N, Armstrong D, Rennie C, Tarnopolsky MA. Substrate utilization during exercise performed with and without glucose ingestion in female and male endurance trained athletes. Int J Sport Nutr Exerc Metab 13: 407–421, 2003.[Web of Science][Medline]
26. Robinson S. Experimental studies of physical fitness in relation to age. Arbeitsphysiologie 10: 251–323, 1938.[CrossRef]
27. Rowland TW, Rimany TA. Physiological responses to prolonged exercise in premenarcheal and adult females. Ped Exerc Sci 7: 183–191, 1995.
28. Rueda-Maza CM, Maffeis C, Zaffanello M, Schutz Y. Total and exogenous carbohydrate oxidation in obese prepubertal children. Am J Clin Nutr 64: 844–849, 1996.[Abstract/Free Full Text]
29. Schoeller DA, Klein PD, Watkins JB, Heim T, MacLean WC Jr. ¹³C abundances of nutrients and the effect of variations in ¹³C isotopic abundances of test meals formulated for ¹³CO₂ breath tests. Am J Clin Nutr 33: 2375–2385, 1980.[Abstract/Free Full Text]
30. Stephens BR, Cole AS, Mahon AD. The influence of biological maturation on fat and carbohydrate metabolism during exercise in males. Int J Sport Nutr Exerc Metab 16: 166–179, 2006.[Web of Science][Medline]
31. Tanner JM. Growth at Adolescence. Oxford, UK: Blackwell Scientific, 1962.
32. Tarnopolsky MA. Gender differences in substrate metabolism during endurance exercise. Can J Appl Physiol 25: 312–327, 2000.[Web of Science][Medline]
33. Timmons BW, Bar-Or O, Riddell MC. Oxidation rate of exogenous carbohydrate during exercise is higher in boys than in men. J Appl Physiol 94: 278–284, 2003.[Abstract/Free Full Text]
34. Timmons BW, Bar-Or O, Riddell MC. Influence of age and pubertal status on substrate utilization during exercise with and without carbohydrate intake in healthy boys. Appl Physiol Nutr Metab 32: 416–425, 2007.[CrossRef][Medline]
35. Timmons BW, Tarnopolsky MA, Snider DP, Bar-Or O. Immunological changes in response to exercise: influence of age, puberty, and gender. Med Sci Sports Exerc 38: 293–304, 2006.
36. Wallis GA, Dawson R, Achten J, Webber J, Jeukendrup AE. Metabolic response to carbohydrate ingestion during exercise in males and females. Am J Physiol Endocrinol Metab 290: E708–E715, 2006.[Abstract/Free Full Text]
37. Wideman L, Consitt L, Patrie J, Swearingin B, Bloomer R, Davis P, Weltman A. The impact of sex and exercise duration on growth hormone secretion. J Appl Physiol 101: 1641–1647, 2006.[Abstract/Free Full Text]

This article has been cited by other articles:

				M. C. Riddell The endocrine response and substrate utilization during exercise in children and adolescents J Appl Physiol, August 1, 2008; 105(2): 725 - 733. [Abstract] [Full Text] [PDF]

				M. C. Riddell, V. K. Jamnik, K. E. Iscoe, B. W. Timmons, and N. Gledhill Fat oxidation rate and the exercise intensity that elicits maximal fat oxidation decreases with pubertal status in young male subjects J Appl Physiol, August 1, 2008; 105(2): 742 - 748. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Free All Versions of this Article: 103/3/995    most recent 00018.2007v1 Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Timmons, B. W. Articles by Riddell, M. C. Search for Related Content PubMed PubMed Citation Articles by Timmons, B. W. Articles by Riddell, M. C.