Endogenous versus exogenous carbohydrate oxidation measured by stable isotopes in pre-pubescent children plus 13C abundances in foods consumed three days prior

Marni E Shoemaker, Zachary M Gillen, Brianna D Mckay, Todd J Leutzinger, Vikkie A Mustad, Joel T Cramer, Marni E Shoemaker, Zachary M Gillen, Brianna D Mckay, Todd J Leutzinger, Vikkie A Mustad, Joel T Cramer

Abstract

Purpose: The purposes of the present study were to (a) examine resting metabolism, substrate utilization, and endogenous versus exogenous carbohydrate (CHO) oxidation before and after 30-g rapidly-digesting carbohydrate (RDC) ingestion using indirect calorimetry and breath test analysis of stable isotope concentrations in pre-pubescent children and (b) report the 13C abundances in foods consumed for three days prior.

Methods: Nineteen children (n = 10 boys, n = 9 girls) at Tanner stage I or II participated (mean age ± 95% CI = 9.84 ± 0.77 y) in this study. Food was administered to the children for three days preceding their scheduled breath tests. Breath tests and indirect calorimetry were performed after an 8-h fast before and 60 min following consumption of a 30-g simple RDC drink consisting of maltodextrin and sucrose. Open circuit spirometry and indirect calorimetry monitored resting metabolism and CHO oxidation. Separate breath samples were taken every 15 min. Samples of all foods and breath samples were analyzed for 13C and 12C abundances with a stable-isotope mass spectrometer.

Results: 13C in expired breath samples were -23.81 ± 1.64‰ at baseline and increased every 15 min after consumption of the CHO drink (p < 0.001-0.009). Cumulative total, endogenous, and exogenous CHO utilization increased during the post-prandial period (p < 0.001). Endogenous CHO oxidation was consistently greater than exogenous CHO oxidation (p < 0.001-0.002).Blood glucose was elevated from baseline at 30- and 60-min post-prandial (p < 0.001). Insulin did not change over time (p = 0.184).

Conclusions: The foods provided during the 3-day controlled diet effectively minimized 13C variation prior to metabolic testing. The 13C abundances of foods reported herein should serve as practical recommendations to reduce 13C intake before breath tests. While endogenous CHO oxidation remained greater in proportion to exogenous CHO oxidation, these findings suggest that even a relatively small amount of RDC can increase exogenous CHO oxidation and blood glucose in normal-weight children. To further examine shifts in endogenous versus exogenous CHO utilization, we recommend that future studies take steps to minimize 13C variation before breath tests and examine changes in substrate metabolism at rest and during exercise in normal weight and overweight pre-pubescent children.

Clinical trial registration number: NCT03185884.

Keywords: 13C abundance; CHO, carbohydrate; Carbohydrate oxidation; DXA, dual-energy x-ray absorptiometry; Pre-pubescent children; RDC, rapidly-digesting carbohydrate; Stable isotopes; Substrate utilization; V̇CO2, rate of carbon dioxide production; V̇O2, rate of oxygen consumption.

Conflict of interest statement

Current disclosures for JTC: From 2001-present, Dr. Cramer’s research has been externally funded by 22 separate project grants from 10.13039/100011947Abbott Nutrition, Nebraska Beef Council, Nebraska Extension, Stepan Lipid Nutrition, Rock Creek Pharmaceuticals, General Nutrition Corporation, Experimental & Applied Sciences, Nutricia, and the University of Nebraska Agriculture Research Division with funds provided by the Hatch Act (Agency: 10.13039/100000199U.S. Department of Agriculture, 10.13039/100005825National Institute for Food and Agriculture: Accession No: 1000080; Project No: NEB-36-078). From 2010 to 2013, Joel was an expert witness or expert consultant in 10 separate legal matters representing defendants Vital Pharmaceuticals, MusclePharm, and Celsius. From 2008 to 2016, Dr. Joel T. Cramer was a paid consultant for either Abbott Nutrition, General Nutrition Center, ErgoGenix/ErgoPharm, and/or Corr-Jensen Labs. From 2018-present, Joel has served as a paid consultant for Regeneron Pharmaceuticals. VAM is an employee and stockholder of Abbott Nutrition. MES, ZMG, BDM, and TJL did not report any potential conflicts of interest.

© 2020 The Authors.

Figures

Fig. 1
Fig. 1
Total carbohydrate (CHO) oxidation broken down as exogenous and endogenous CHO oxidation cumulatively across 60 min in pre-pubescent children before and after consuming a 30-g rapid-digesting carbohydrate (RDC) drink.
Fig. 2
Fig. 2
Means ± 95% Confidence Intervals of glucose (closed circles) and insulin (open circles) responses of pre-pubescent children (n = 19) measured at baseline and 30 and 60 min after consuming a 30-g RDC drink.

References

    1. Who . World Health Organization; Geneva: 2015. Guideline: sugars intake for adults and children. [cited 2020 Jan 6]. Available from:
    1. Malik V.S., Schulze M.B., Hu F.B. Intake of sugar-sweetened beverages and weight gain: a systematic review. Am J Clin Nutr. 2006 Aug;84(2):274–288.
    1. Stanhope K.L. Sugar consumption, metabolic disease and obesity: the state of the controversy. Crit Rev Clin Lab Sci. 2016 Feb;53(1):52–67.
    1. Malik V.S., Pan A., Willett W.C., Hu F.B. Sugar-sweetened beverages and weight gain in children and adults: a systematic review and meta-analysis123. Am J Clin Nutr. 2013 Oct;98(4):1084–1102.
    1. Vartanian L.R., Schwartz M.B., Brownell K.D. Effects of soft drink consumption on nutrition and health: a systematic review and meta-analysis. Am J Publ Health. 2007 Apr;97(4):667–675.
    1. Mattes R.D., Shikany J.M., Kaiser K.A., Allison D.B. Nutritively sweetened beverage consumption and body weight: a systematic review and meta-analysis of randomized experiments. Obes Rev. 2011 May;12(5):346–365.
    1. Bosy-Westphal A., Hägele F., Nas A. Impact of dietary glycemic challenge on fuel partitioning. Eur J Clin Nutr. 2017;71(3):327–330.
    1. Schoeller D.A., Schneider J.F., Solomons N.W., Watkins J.B., Klein P.D. Clinical diagnosis with the stable isotope 13C in CO2 breath tests: methodology and fundamental considerations. J Lab Clin Med. 1977 Sep;90(3):412–421.
    1. Achten J., Jentjens R.L., Brouns F., Jeukendrup A.E. Exogenous oxidation of isomaltulose is lower than that of sucrose during exercise in men. J Nutr. 2007 May;137(5):1143–1148.
    1. Normand S., Pachiaudi C., Khalfallah Y., Guilluy R., Mornex R., Riou J.P. 13C appearance in plasma glucose and breath CO2 during feeding with naturally 13C-enriched starchy food in normal humans. Am J Clin Nutr. 1992 Feb;55(2):430–435.
    1. Riddell M.C., Partington S.L., Stupka N., Armstrong D., Rennie C., Tarnopolsky M.A. Substrate utilization during exercise performed with and without glucose ingestion in female and male endurance trained athletes. Int J Sport Nutr Exerc Metabol. 2003 Dec;13(4):407–421.
    1. Wagenmakers A.J., Brouns F., Saris W.H., Halliday D. Oxidation rates of orally ingested carbohydrates during prolonged exercise in men. J Appl Physiol. 1993 Dec;75(6):2774–2780.
    1. Leites G.T., Cunha G.S., Chu L., Meyer F., Timmons B.W. Energy substrate utilization with and without exogenous carbohydrate intake in boys and men exercising in the heat. J Appl Physiol. 2016 01;121(5):1127–1134.
    1. Rueda-Maza C.M., Maffeis C., Zaffanello M., Schutz Y. Total and exogenous carbohydrate oxidation in obese prepubertal children. Am J Clin Nutr. 1996 Dec;64(6):844–849.
    1. Timmons B.W., Bar-Or O., Riddell M.C. Energy substrate utilization during prolonged exercise with and without carbohydrate intake in preadolescent and adolescent girls. J Appl Physiol. 2007 Sep;103(3):995–1000.
    1. Timmons B.W., Bar-Or O., Riddell M.C. Influence of age and pubertal status on substrate utilization during exercise with and without carbohydrate intake in healthy boys. Appl Physiol Nutr Metabol. 2007 Jun;32(3):416–425.
    1. Schoeller D.A., Klein P.D., Watkins J.B., Heim T., MacLean W.C. 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. 1980 Nov;33(11):2375–2385.
    1. Jahren A.H., Saudek C., Yeung E.H., Kao W.H.L., Kraft R.A., Caballero B. An isotopic method for quantifying sweeteners derived from corn and sugar cane. Am J Clin Nutr. 2006 Dec;84(6):1380–1384.
    1. Marshall J.D., Brooks J.R., Lajtha K. John Wiley & Sons, Ltd; 2008. Sources of variation in the stable isotopic composition of plants. Stable isotopes in ecology and environmental science; pp. 22–60.
    1. Marshall W.A., Tanner J.M. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969 Jun;44(235):291–303.
    1. Marshall W.A., Tanner J.M. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970 Feb;45(239):13–23.
    1. Warburton D.E.R., Jamnik V.K., Bredin S.S.D., Gledhill N. The physical activity readiness Questionnaire for everyone (PAR-Q+) and electronic physical activity readiness medical examination (ePARmed-X+): summary of consensus panel recommendations. The Health & Fitness J Can. 2011 Aug;4(2):26–37.
    1. Mirwald R.L., Baxter-Jones A.D.G., Bailey D.A., Beunen G.P. An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc. 2002 Apr;34(4):689–694.
    1. Frayn K.N. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol Respir Environ Exerc Physiol. 1983 Aug;55(2):628–634.
    1. Jeukendrup A.E., Wallis G.A. Measurement of substrate oxidation during exercise by means of gas exchange measurements. Int J Sports Med. 2005 Feb;26(Suppl 1):S28–S37.
    1. Craig H. The geochemistry of the stable carbon isotopes. Geochem Cosmochim Acta. 1953 Feb;3(2):53–92.
    1. 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. Metab Clin Exp. 1976 Dec;25(12):1575–1582.
    1. Hales C.M., Carroll M.D., Fryar C.D., Ogden C.L. 2019 Jun. Prevalence of obesity among adults and youth: United States, 2015-2016. [Internet] [cited 2020 Jan 7]. Available from:
    1. Skinner A.C., Ravanbakht S.N., Skelton J.A., Perrin E.M., Armstrong S.C. Prevalence of obesity and severe obesity in US children, 1999–2016. Pediatrics. 2018 Mar;141(3) doi: 10.1542/peds.2017-3459.
    1. Roach P.J. Glycogen and its metabolism. Curr Mol Med. 2002 Mar;2(2):101–120.
    1. Eckel R.H., Hernandez T.L., Bell M.L., Weil K.M., Shepard T.Y., Grunwald G.K. Carbohydrate balance predicts weight and fat gain in adults. Am J Clin Nutr. 2006 Apr;83(4):803–808.
    1. Højlund K., Beck-Nielsen H. Impaired glycogen synthase activity and mitochondrial dysfunction in skeletal muscle: markers or mediators of insulin resistance in type 2 diabetes? Curr Diabetes Rev. 2006 Nov;2(4):375–395.

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する