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Breath [¹³CO₂] recovery from an oral glucose load during exercise: comparison between [U-¹³C] and [1,2-¹³C]glucose

¹Département de kinésiologie, Université de Montréal, CP 6128 Centre Ville, Montréal H3C 3J7; ²Département de kinanthropologie, Université du Québec à Montréal, Montréal H3C 3P8; and ³Département des Sciences de l'activité physique, Université du Québec à Trois Rivières, Trois Rivières, Québec, Canada G9A 5H7

Submitted 30 January 2003 ; accepted in final form 31 March 2003

	ABSTRACT

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The purpose of the present experiment was to compare ¹³CO₂ recovery at the mouth, and the corresponding exogenous glucose oxidation computed, during a 100-min exercise at 63 ± 3% maximal O₂ uptake with ingestion of glucose (1.75 g/kg) in six active male subjects, by use of [U-¹³C] and [1,2-¹³C]glucose. We hypothesized that ¹³C recovery and exogenous glucose oxidation could be lower with [1,2-¹³C] than [U-¹³C]glucose because both tracers provide ^[13C]acetate, with possible loss of ¹³C in the tricarboxylic acid (TCA) cycle, but decarboxylation of pyruvate from [U-¹³C]glucose also provides ¹³CO₂, which is entirely recovered at the mouth during exercise. The recovery of ¹³C (25.8 ± 2.3 and 27.4 ± 1.2% over the exercise period) and the amounts of exogenous glucose oxidized computed were not significantly different with [1,2-¹³C] and [U-¹³C]glucose (28.9 ± 2.6 and 30.7 ± 1.3 g, between minutes 40 and 100), suggesting that no significant loss of ¹³C occurred in the TCA cycle. This stems from the fact that, during exercise, the rate of exogenous glucose oxidation is probably much larger than the flux of the metabolic pathways fueled from TCA cycle intermediates. It is thus unlikely that a significant portion of the ¹³C entering the TCA cycle could be diverted to these pathways. From a methodological standpoint, this result indicates that when a large amount of [¹³C]glucose is ingested and oxidized during exercise, ¹³CO₂ production at the mouth accurately reflects the rate of glucose entry in the TCA cycle and that no correction factor is needed to compute the oxidative flux of exogenous glucose.

stable isotopes; indirect respiratory calorimetry; energy metabolism; substrate oxidation

View larger version (23K): [in this window] [in a new window]   Fig. 1. Metabolic fate of carbon atoms provided by [U-*C]glucose. Carbons 3 and 4 (carbon 1 in pyruvate) released as CO2 upstream acetate, do not enter the tricarboxylic acid (TCA) cycle. Carbons 2 and 5 entering the TCA cycle in position 1 on [U-*C]acetate provide CO2 at the second turn of the cycle: 50% before + 50% after -ketoglutarate (because of randomization of carbons in the succinate molecule). Carbons 1 and 6 entering the TCA cycle in position 2 in [U-*C]acetate, provides CO2 beginning at the third turn of the cycle: 25% before + 25% after -ketoglutarate at the third turn; 12.5% + 12.5% at the fourth turn, and so on (for the detailed pathways followed by the carbons in the TCA cycle see, e.g., Ref. 26). Carbons entering the TCA cycle could also be incorporated into 1) fatty acids from citrate; 2) glutamate from a-ketoglutarate; 3) glucose from malate (with partial recovery of isotope as labeled CO2); and 4) aspartate from oxaloacetate (see, e.g., Ref. 25).

The purpose of the present experiment was to verify this hypothesis by comparing ¹³C recovery under CO₂ at the mouth and exogenous glucose oxidation during prolonged exercise at moderate workload by using [U-¹³C] and [1,2-¹³C]glucose as tracers. Under the hypothesis that a significant amount of ¹³C provided in the form of acetate is irreversibly lost in the TCA cycle, ¹³C recovery at the mouth and the exogenous glucose oxidation computed will be lower with [1,2-¹³C] than with [U-¹³C]glucose. This is due to the fact that both [1,2-¹³C] and [U-¹³C]glucose provide [¹³C]acetate, with possible loss of ¹³C in the TCA cycle, but that decarboxylation of pyruvate into acetate from [U-¹³C]glucose also provides ¹³CO₂ that is entirely recovered at the mouth during exercise (12, 23, 25).

	METHODS

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Subjects. The experiment was conducted on six active and healthy male subjects who gave their informed, written consent to participate in the study, which was approved by the Institutional Board on the Use of Human Subjects in Research. None of the subjects were smokers, heavy drinkers, under medication, or using recreational drugs. Their age, weight, and maximal O₂ uptake (O_{2 max}) on a cycle ergometer (Ergomeca, La Bayette, France) were 25.3 ± 1.1 yr, 64.1 ± 1.9 kg, and 61.2 ± 2.7 ml · kg ^-1 · min^-1, respectively (means ± SE).

Experiments. O_{2 max} and experimental workload on the cycle ergometer were determined for each subject during a preliminary test session using open-circuit spirometry (1100 medical gas analyzer, Marquette Electronics, Milwaukee, WI). Subsequently, all subjects performed at 1-wk intervals, between 10:00 AM and 12:00 noon, three exercises of 100-min duration on a cycle ergometer at 178 ± 10 W, corresponding to 60% of the maximal workload (297 ± 16 W), and 63 ± 3% O_{2 max}. The last evening meal before each experiment (7:00 PM; 1,250 kcal: 70% carbohydrates, 15% lipids, 15% proteins) and the morning breakfast (7:30 AM; 500 kcal: 50% carbohydrates, 35% lipids, 15% proteins) were standardized and were poor in ¹³C. In addition, to keep a low background ¹³C enrichment of expired CO₂, ingestion of carbohydrates from plants with the C₄ photosynthetic cycle, which are naturally enriched in ¹³C (13), was avoided 1 wk before and during the period of experiments. Subjects also refrained from exercising and from drinking coffee and alcohol for 2 days before each experiment.

¹³C labeling. During the experiments, the subjects ingested, in a single-blind random fashion, 1.75 g/kg body mass of either [U-¹³C]- or [1,2-¹³C]-enriched glucose or a placebo (artificial low-calorie sweetener: aspartame, Nabisco, Etobicoke, ON, Canada) dissolved in water (21 ml/kg). The solution was ingested as follows: 6 ml/kg with the placebo or 0.50 g of glucose/kg 20 min before the beginning of exercise; 3 ml/kg with the placebo or 0.25 g of glucose/kg every 20 min thereafter, up to minute 80. The subjects ingested a total of 1,346 ± 40 ml of water without glucose or with 112 ± 4 g of glucose. The glucose, which was naturally poor in ¹³C [Avebe America, Princeton, NJ; ¹³C-to-¹²C ratio (¹³C/¹²C) = -25.2 ¹³C Pee Dee Belemnitella-1 (PDB-1)], was artificially enriched either with [U-¹³C] or [1,2-¹³C]glucose (¹³C/¹²C > 99% on the labeled carbons; Isotec, Miamisburg, OH) to achieve final isotopic compositions ranging between 15 and 20 ¹³C PDB-1. No attempt was made to exactly match the isotopic compositions of the ingested glucose; actual values measured by mass spectrometry were + 17.3 and + 13.3 ¹³C PDB-1 for [U-¹³C] and [1,2-¹³C]glucose, respectively.

Measurements and analysis. Measurements were made at rest before ingestion of the first dose of glucose and every 20 min during the exercise period. The isotopic composition of expired CO₂ was measured by continuous-flow mass spectrometry (Isoprime, Micromass, Manchester, UK) in 10-ml samples of expired gases collected in vacutainers (Becton-Dickinson, Franklin Lakes, NJ). The ¹³C/¹²C was expressed in difference by comparison with the Chicago PDB-1 standard: ¹³C PDB-1 = [(Rspl/Rstd) -1] x 1,000, where Rspl and Rstd are ¹³C/¹²C in the sample and standard (1.1237%), respectively (4). CO₂ production was measured along with O₂ consumption by open circuit spirometry (1100 medical gas analyzer, Marquette Electronics, Milwaukee, WI). The cumulative amount of ¹³C recovered in the form of ¹³CO₂ at the mouth was computed every 20 min from the beginning of exercise, from the cumulative volume of ¹³CO₂ produced and the cumulative amount of ¹³C in the glucose ingested. The oxidation rate of exogenous glucose (g/min) was then computed as follows (18)

Exogenous glucose

(1)

where CO₂ is CO₂ production (in l/min), Rexp is ¹³C/¹²C observed in expired CO₂, Rref is ¹³C/¹²C in expired CO₂ during exercise without glucose ingestion, Rexo is ¹³C/¹²C in the exogenous glucose ingested, and k is the volume of CO₂ provided by the complete oxidation of glucose (0.7426 l/g). As indicated in the introduction, this computation underestimates glucose oxidation at the beginning of exercise because ¹³C/¹²C in expired CO₂ only slowly equilibrates with ¹³C/¹²C in the CO₂ produced in tissues (16). For this reason, the computations were made beginning at minute 40 during the exercise period.

Statistics. Data are presented as means ± SE. Comparisons between the two experimental situations were made by using analysis of variance for repeated measurements (Statistica package; StatSoft, Tulsa, OK). Newman-Keuls post hoc tests were used to identify the location of significant differences (P 0.05) when the analysis of variance yielded a significant F ratio.

	RESULTS

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No significant difference was observed for O₂ consumption in response to exercise with ingestion of the placebo or [U-¹³C] or [1,2-¹³C]glucose, but the respiratory exchange ratio was higher beginning at minute 60 when glucose was ingested (Table 1). Table 1 also shows ¹³C/¹²C in expired CO₂ at rest before exercise and before ingestion of the placebo or [¹³C]glucose. No significant difference was observed for the basal values of ¹³C/¹²C in expired CO₂ before ingestion of the placebo or ¹³C glucose. As expected, a small transient increase in ¹³C/¹²C in expired CO₂ was observed in response to exercise with ingestion of the placebo (18). In contrast, ¹³C/¹²C in expired CO₂ markedly and steadily increased throughout the exercise period when [¹³C]glucose was ingested. The increase was larger with ingestion of [U-¹³C] than [1,2-¹³C]glucose, but changes in ¹³C/¹²C in expired CO₂ cannot be directly compared in these two situations because ¹³C/¹²C was also slightly higher in [U-¹³C] than in [1,2-¹³C] ingested glucose (+17.3 and +13.3 ¹³C PDB-1, respectively). The recovery of ¹³C in the form of ¹³CO₂ at the mouth, in percent of the amount ingested, was similar with [U-¹³C] or [1,2-¹³C]glucose (Fig. 2).

View this table: [in this window] [in a new window]   Table 1. O2, RER, and 13C/12C of expired CO2 in response to exercise

View larger version (14K): [in this window] [in a new window]   Fig. 2. Recovery of 13C in expired CO2 at the mouth (% of 13C ingested) in response to exercise with ingestion of the placebo or [13C]glucose (A), and oxidation rate of exogenous glucose at 20-min intervals beginning at minute 40 during the exercise period (B).

Exogenous glucose oxidation computed at 20-min intervals during the exercise period, beginning at minute 40 (Fig. 2), and the cumulative amounts of exogenous glucose oxidized between minutes 40 and 100 (28.9 ± 2.6 and 30.7 ± 1.3 g with [1,2-¹³C] and [U-¹³C]glucose, respectively) were not significantly different in the two experimental situations. A high and significant correlation coefficient (r = 0.965) was observed between the individual values of exogenous glucose oxidation rates computed at 20-min intervals between minutes 40 and 100 with [U-¹³C] and [1,2-¹³C] ingested glucose (Fig. 3).

View larger version (12K): [in this window] [in a new window]   Fig. 3. Individual values for the oxidation of exogenous glucose at 20-min intervals beginning at minute 40 during the exercise period, computed by using [U-13C]glucose, plotted against the corresponding values computed by using [1,2-13C]glucose. The regression line is shown (r = 0.965, n = 24, P < 0.05).

	DISCUSSION

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Results from the present experiment indicate that when a large amount of [¹³C]glucose is ingested and oxidized during prolonged moderate exercise, ¹³C recovery at the mouth, and, hence, the exogenous glucose oxidation computed, are similar when [U-¹³C] or [1,2-¹³C]glucose is ingested. This observation suggests that, in this situation, no significant loss of ¹³C provided by [¹³C]glucose occurs in the TCA cycle.

Carbon atoms entering the TCA cycle not only provide CO₂ and bicarbonate but could also be incorporated in metabolic pathways that are fueled from the pools of TCA cycle intermediates, such as gluconeogenesis from malate, aspartate synthesis from oxaloacetate, glutamate synthesis from oxoglutarate, and fatty acid synthesis from citrate (19, 22, 24) (Fig. 1). As a consequence, when a substrate providing carbon to the TCA cycle is labeled with ¹³C or ¹⁴C, label CO₂ production at the mouth could underestimate its "oxidation," i.e., decarboxylation and dehydrogenation of the substrate, and supply of reducing equivalents to the respiratory chain.

This phenomenon, which has been originally shown in vivo at rest by Wolfe and Jahoor (29), has been consistently reported at rest, with recovery values ranging from 45 to 81% for label in position 1 and 23–65% for label in position 2 of the acetate molecule (Table 2). This difference stems from the fact that carbon 1 in acetate provides CO₂ at the second turn of the TCA cycle, whereas carbon 2 only provides CO₂ beginning at the third turn (19, 26, 29) (see Fig. 1). Accordingly, there is a greater chance for carbon 2 than carbon 1 to be removed from the pool of TCA cycle intermediates before provision of CO₂. Data from Pouteau et al. (19) and Schrauwen et al. (22) observed at rest indicate that 30% of the labeled acetate underwent nonoxidative disposal (19); 5 (19) to 12% (22) were recovered in the form of glutamine, with an additional portion in the form of glutamate 10% (22); and 1.6–6.4% were recovered in the form of glucose, when [1-¹³C] and [2-¹³C]acetate, respectively, were infused (19). In addition, Pouteau et al. (19) estimated that between 6 and 12% could have been incorporated into pyruvate and aspartate. In the study by Schneiter et al. (20), an equimolar mixture of [1-¹³C]acetate, [2-¹³C]acetate, and NaH¹³CO₃ was infused, thus mimicking the fate of carbon isotope from [U-¹³C]glucose. The overall recovery factor measured (54%) is in good agreement with that computed from data measured separately by Trimmer et al. (25), at rest, for each of the three compounds [(50 + 26 + 77)/3 = 51%] (Table 2). In addition, in both studies, the increase in labeled carbon observed from rest to exercise was also similar: 76–79% (20, 25) due to a higher recovery from both [1-¹³C] (80%) and [2-¹³C]acetate (65%) (25).

The difference in carbon isotope loss in the TCA cycle between [2-^* C] and [1-^* C]acetate (Fig. 1) explains that the oxidation rate of fatty acids computed at rest from labeled CO₂ production at the mouth is 30–50% lower with the carbon isotope in odd than even position (3, 5, 14). However, in these studies, labeled fatty acids were ingested (3, 5) or infused (14) in trace amounts (100–700 mg). No data are available on possible isotope loss from fatty acids labeled in different positions when ingested in larger amounts. As for the differential fate of carbon isotope provided by a large glucose amount (75 g), on the basis of data concerning carbon isotope loss in the TCA cycle, Féry et al. (6) hypothesized that ¹⁴C recovery in the form of CO₂ and hence exogenous glucose oxidation computed at rest could be larger with [U-¹⁴C] than [1-¹⁴C]glucose. We also hypothesized that the same phenomenon can occur in response to prolonged exercise with ingestion of a large amount of [U-¹³C] or [1,2-¹³C]glucose. For example, on the basis of the recovery factors reported by Trimmer et al. (25) for [1-¹³C] (80%) and [2-¹³C]acetate (65%) during exercise, and with the assumption of a complete recovery of carbon isotope released between pyruvate and acetate, exogenous glucose oxidation computed by using [U¹³-C]glucose ([100 + 80 + 65]/3) could be expected to be 12% higher than that computed by using [1,2-¹³C]glucose ([80 + 65]/2).

This hypothesis, however, was not supported by the observations made in the study by Féry et al. (6) nor in the present experiment. In the study by Féry et al., ¹⁴CO₂ recovery at the mouth and exogenous glucose oxidation computed after a 14-h fast were similar at rest with [U-¹⁴C] and [1-¹⁴C]glucose (27%, and 20 g over 5 h). Data from the present experiment indicate that ¹³CO₂ recovery at the mouth over the 100-min exercise period were not significantly different when [1,2-¹³C] and [U-¹³C]glucose were ingested (25.8 ± 2.3 and 27.4 ± 1.2%). As a consequence, the amounts of exogenous glucose oxidized that were computed were not significantly different and were, in fact, very close (28.9 ± 2.6 and 30.7 ± 1.3 g with [1,2-¹³C] and [U-¹³C]glucose, respectively, between minutes 40 and 100).

These consistent observations from Féry et al. (6) and from the present experiment differ from those reported by several authors that have shown an incomplete recovery of carbon isotope in the form of labeled CO₂ when labeled acetate was administered (Table 2). The most likely explanation is that in all these studies the amounts of labeled substrate administered was very small (e.g., 2–8 mg/min in humans). In this situation, it is well possible that the flux of ¹³C entering the TCA cycle was within the range of the flux through the pathways originating from TCA intermediates, such as gluconeogenesis, glutamate and aspartate synthesis, and fatty acid synthesis. Accordingly, a significant portion of the flux of labeled acetate could be diverted to these pathways. In contrast, in the present experiment, the oxidative flux of exogenous glucose, which ranged between 0.2 g/min (at minute 40) and 0.7 g/min (at minute 100), was two orders of magnitude larger than the infusion rates used in the studies summarized in Table 2. It is thus much less likely that a significant portion of the ¹³C entering the TCA cycle could be diverted to these pathways. In addition, the present experiment was performed at exercise. In this situation, plasma and exogenous glucose are mainly metabolized in active muscles where glucose and fatty acid synthesis are unlikely to occur. Indeed, Schrauwen et al. (22), Sidossis et al. (23), and Trimmer et al. (25) have reported a large increase in carbon isotope recovery from labeled acetate from rest to exercise (Table 2).

From a methodological standpoint, this result indicates that when a large amount of [¹³C]glucose labeled in position 1 and/or 2 (or 5 and/or 6) or uniformly labeled is ingested and oxidized during exercise, ¹³C production at the mouth accurately reflects the rate of glucose entry in the TCA cycle. Thus no correction factor is needed to compute the oxidative flux of exogenous glucose.

	DISCLOSURES

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This study was supported by a grant from the Natural Sciences and Engineering Research Council of Canada and by the Centre de Recherche en Géochimie Isotopique et Géodynamique (UQAM-McGill).

	FOOTNOTES

 

Address for reprint requests and other correspondence: D. Massicotte, Département de kinanthropologie, Université du Québec à Montréal, CP 8888, Succursale Centre-Ville, Montréal, P.Q., Canada H3C 3P8 (E-mail: massicotte.denis{at}uqam.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.

	REFERENCES

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1. Barstow TJ, Cooper DM, Epstein S, and Wasserman K. Changes in breath ¹³CO₂/¹²CO₂ consequent to exercise and hypoxia. J Appl Physiol 66: 936-942, 1989.[Abstract/Free Full Text]
2. Bäurle W, Brösicke H, Matthews DE, Pogan K, and Fürst P. Metabolism of parenterally administered fat emulsions in the rat: studies of fatty acid oxidation with 1-¹³C- and 8-¹³C-labelled triolein. Br J Nutr 79: 381-387, 1998.[Web of Science][Medline]
3. Clandinin MT, Khetarpal S, Kielo ES, French MA, Tokarska B, and Goh YK. Chain shortening of palmitic acid in human subjects. Am J Clin Nutr 48: 587-591, 1988.[Abstract/Free Full Text]
4. Craig H. The geochemistry of the stable carbon isotopes. Geochim Cosmochim Acta 3: 53-92, 1953.
5. DeLany JP, Windhauser MM, Champagne CM, and Bray GA. Differential oxidation of individual dietary fatty acids in humans. Am J Clin Nutr 72: 905-911, 2000.[Abstract/Free Full Text]
6. Féry F, Plat L, and Balasse EO. Mechanism of whole-body glycogen deposition after oral glucose in normal subjects. Influence of the nutritional status. J Clin Endocrinol Metab 83: 2810-2816, 1998.[Abstract/Free Full Text]
7. Folch N, Péronnet F, Massicotte D, Duclos M, Lavoie C, and Hillaire-Marcel C. Metabolic response to small and large ¹³C-labelled pasta meals following rest or exercise in man. Br J Nutr 85: 671-680, 2001.[Web of Science][Medline]
8. Hawley JA, Dennis SC, and Noakes TD. Oxidation of carbohydrate ingested during prolonged endurance exercise. Sports Med 14: 27-42, 1992.[Web of Science][Medline]
9. Hoerr RA, Yu Y-M, Wagner DA, Burke JF, and Young VR. Recovery of ¹³C in breath from NaH¹³CO₃ infused by gut and vein: effect of feeding. Am J Physiol Endocrinol Metab 257: E426-E438, 1989.[Abstract/Free Full Text]
10. Irving CS, Wong WW, Shulman RJ, Smith EO, and Klein PD. [¹³C] bicarbonate kinetics in humans: intra- vs. interindividual variations. Am J Physiol Regul Integr Comp Physiol 245: R190-R202, 1983.[Abstract/Free Full Text]
11. Jeukendrup AE and Jentjens R. Oxidation of carbohydrate feedings during prolonged exercise. Current thoughts, guidelines and directions for future research. Sports Med 29: 407-424, 2000.[Web of Science][Medline]
12. Leese GP, Nicoll AE, Varnier M, Thompson J, Scrimgeour CM, and Rennie MJ. Kinetics of ¹³CO₂ elimination after ingestion of ¹³C bicarbonate: the effects of exercise and acid base balance. Eur J Clin Invest 24: 818-823, 1994.[Web of Science][Medline]
13. Lefèbvre PJ. From plant physiology to human metabolic investigations. Diabetologia 28: 255-263, 1985.[Web of Science][Medline]
14. Metges CC and Wolfram G. Different ¹³CO₂ recovery of orally administrated [1-¹³C] and [8-¹³C] triolein in postprandial humans: an effect of phosphoenolpyruvate-carboxykinase (EC 4.1.1.32 [EC] ) in peripheral tissues? Clin Nutr 12: 337-343, 1993.
15. Mittendorfer B, Sidossis LS, Walser E, Chinkes DL, and Wolfe RR. Regional acetate kinetics and oxidation in human volunteers. Am J Physiol Endocrinol Metab 274: E978-E983, 1998.[Abstract/Free Full Text]
16. Pallikaris N, Sphiris N, and Lefèvre PJ. Influence of the bicarbonate pool on the occurrence of ¹³CO₂ in exhaled air. Eur J Appl Physiol 63: 179-183, 1991.
17. Péronnet F, Adopo E, Massicotte D, and Hillaire-Marcel C. Exogenous substrate oxidation during exercise: studies using isotopic labelling. Int J Sports Med 13: S123-S125, 1992.
18. Péronnet F, Massicotte D, Brisson G, and Hillaire-Marcel C. Use of ¹³C-substrates for metabolic studies in exercise: methodological considerations. J Appl Physiol 69: 1047-1052, 1990.[Abstract/Free Full Text]
19. Pouteau E, Maugère P, Darmaun D, Marchini JS, Piloquet H, Dumon H, Nguyen P, and Krempf M. Role of glucose and glutamine synthesis in the differential recovery of ¹³CO₂ from infused [2-¹³C] vs. [1-¹³C] acetate. Metabolism 47: 549-554, 1998.[Web of Science][Medline]
20. Schneiter P, Di Vetta V, Jéquier E, and Tappy L. Effect of physical exercise on glycogen turnover and net substrate utilization according to the nutritional state. Am J Physiol Endocrinol Metab 269: E1031-E1036, 1995.[Abstract/Free Full Text]
21. Schrauwen P, Blaak EE, van Aggel-Leijssen DPC, Borghouts LB, and Wagenmakers AJM. Determinants of the acetate recovery factor: implications for estimation of [U-¹³C] substrate oxidation. Clin Sci (Lond) 98: 587-592, 2000.[Medline]
22. Schrauwen P, van Aggel-Leijssen DPC, van Marken Lichtenbelt WD, van Baak MA, Gijsen AP, and Wagenmakers AJM. Validation of the [1,2-¹³C] acetate recovery factor for correction of [U-¹³C] palmitate oxidation rates in humans. J Physiol 513: 215-223, 1998.[Abstract/Free Full Text]
23. Sidossis LS, Coggan AR, Gastaldelli A, and Wolfe RR. A new correction factor for use in tracer estimations of plasma fatty acid oxidation. Am J Physiol Endocrinol Metab 269: E649-E656, 1995.[Abstract/Free Full Text]
24. Sidossis LS, Coggan AR, Gastaldelli A, and Wolfe RR. Pathway of free fatty acid oxidation in human subjects. J Clin Invest 95: 278-284, 1995.[Web of Science][Medline]
25. Trimmer JK, Casazza GA, Horning MA, and Brooks GA. Recovery of ¹³CO₂ during rest and exercise after [1-¹³C]acetate, [2-¹³C]acetate, and NaH¹³CO₃ infusions. Am J Physiol Endocrinol Metab 281: E683-E692, 2001.[Abstract/Free Full Text]
26. Van Hall G. Correction factors for ¹³C-labelled substrate oxidation at whole-body and muscle level. Proc Nutr Soc 58: 979-986, 1999.[Web of Science][Medline]
27. Wolfe RR. Isotopic measurement of glucose and lactate kinetics. Ann Med 22: 163-170, 1990.[Web of Science][Medline]
28. Wolfe RR. Radioactive and Stable Isotope Tracers in Biomedicine. New York: Wiley-Liss, 1992, p. 251-254.
29. Wolfe RR and Jahoor F. Recovery of labeled CO₂ during infusion of C-1 vs. C-2-labeled acetate: implications for tracer studies of substrate oxidation. Am J Clin Nutr 51: 248-252, 1990.[Abstract/Free Full Text]

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