High-precision mass spectrometric analysis using stable isotopes in studies of children
Corresponding Author
Henk Schierbeek
Division of Neonatology, Department of Pediatrics, Erasmus MC—Sophia Children's Hospital, P.O. Box 2060, 3000 CB Rotterdam, The Netherlands
Department of Pediatrics, VU University Medical Center, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands
Department of Pediatrics, Emma Children's Hospital—AMC, P.O. Box 22660, 1100 DD Amsterdam, The Netherlands
Division of Neonatology, Department of Pediatrics, Erasmus MC—Sophia Children's Hospital, P.O. Box 2060, 3000 CB Rotterdam, The Netherlands.Search for more papers by this authorChris H.P. van den Akker
Division of Neonatology, Department of Pediatrics, Erasmus MC—Sophia Children's Hospital, P.O. Box 2060, 3000 CB Rotterdam, The Netherlands
Search for more papers by this authorLaurent B. Fay
Department of Nutrition and Health, Nestlé Research Center, Nestec Ltd, P.O. Box 44, CH-1000 Lausanne 26, Switzerland
Search for more papers by this authorJohannes B. van Goudoever
Department of Pediatrics, VU University Medical Center, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands
Department of Pediatrics, Emma Children's Hospital—AMC, P.O. Box 22660, 1100 DD Amsterdam, The Netherlands
Search for more papers by this authorCorresponding Author
Henk Schierbeek
Division of Neonatology, Department of Pediatrics, Erasmus MC—Sophia Children's Hospital, P.O. Box 2060, 3000 CB Rotterdam, The Netherlands
Department of Pediatrics, VU University Medical Center, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands
Department of Pediatrics, Emma Children's Hospital—AMC, P.O. Box 22660, 1100 DD Amsterdam, The Netherlands
Division of Neonatology, Department of Pediatrics, Erasmus MC—Sophia Children's Hospital, P.O. Box 2060, 3000 CB Rotterdam, The Netherlands.Search for more papers by this authorChris H.P. van den Akker
Division of Neonatology, Department of Pediatrics, Erasmus MC—Sophia Children's Hospital, P.O. Box 2060, 3000 CB Rotterdam, The Netherlands
Search for more papers by this authorLaurent B. Fay
Department of Nutrition and Health, Nestlé Research Center, Nestec Ltd, P.O. Box 44, CH-1000 Lausanne 26, Switzerland
Search for more papers by this authorJohannes B. van Goudoever
Department of Pediatrics, VU University Medical Center, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands
Department of Pediatrics, Emma Children's Hospital—AMC, P.O. Box 22660, 1100 DD Amsterdam, The Netherlands
Search for more papers by this authorAbstract
The use of stable isotopes combined with mass spectrometry (MS) provides insight into metabolic processes within the body. Herein, an overview on the relevance of stable isotope methodology in pediatric research is presented. Applications for the use of stable isotopes with MS cover carbohydrate, fat, and amino acid metabolism as well as body composition, energy expenditure, and the synthesis of specific peptides and proteins, such as glutathione and albumin. The main focus of these studies is on the interactions between nutrients and the endogenous metabolism within the body and how these factors affect the health of a growing infant. Considering that the early imprinting of metabolic processes hugely impacts metabolism (and thus functional outcome) later in life, research in this area is important and is advancing rapidly. The major fluxes on a metabolic level are the synthesis and breakdown rates. They can be quantified using kinetic tracer analysis and mathematical modeling. Organic MS and isotope ratio mass spectrometry (IRMS) are the two most mature techniques for the isotopic analysis of compounds. Introduction of the samples is usually done by coupling gas chromatography (GC) to either IRMS or MS because it is the most robust technique for specific isotopic analysis of volatile compounds. In addition, liquid chromatography (LC) is now being used more often as a tool for sample introduction of both volatile and non-volatile compounds into IRMS or MS for 13C isotopic analyses at natural abundances and for 13C-labeled enriched compounds. The availability of samples is often limited in pediatric patients. Therefore, sample size restriction is important when developing new methods. Also, the availability of stable isotope-labeled substrates is necessary for measurements of the kinetics and concentrations in metabolic studies, which can be a limiting factor. During the last decade, the availability of these substrates has increased. Furthermore, improvements in the accuracy, precision, and sensitivity of existing techniques (such as GC/IRMS) and the development of new techniques (such as LC/IRMS) have opened up new avenues for tackling these limitations. © 2011 Wiley Periodicals, Inc. Mass Spec Rev 31:312–330, 2012
REFERENCES
- Abramson FP, Black GE, Lecchi P. 2001. Application of high-performance liquid chromatography with isotope-ratio mass spectrometry for measuring low levels of enrichment of underivatized materials. J Chromatogr A 913: 269–273.
- Agostoni C, Buonocore G, Carnielli VP, De Curtis M, Darmaun D, Decsi T, Domellof M, Embleton ND, Fusch C, Genzel-Boroviczeny O, Goulet O, Kalhan SC, Kolacek S, Koletzko B, Lapillonne A, Mihatsch W, Moreno L, Neu J, Poindexter B, Puntis J, Putet G, Rigo J, Riskin A, Salle B, Sauer P, Shamir R, Szajewska H, Thureen P, Turck D, van Goudoever JB, Ziegler EE. 2010. Enteral nutrient supply for preterm infants: Commentary from the European Society of Paediatric Gastroenterology, Hepatology and Nutrition Committee on Nutrition. J Pediatr Gastroenterol Nutr 50: 85–91.
- Alamdari DH, Kostidou E, Paletas K, Sarigianni M, Konstas AG, Karapiperidou A, Koliakos G. 2005. High sensitivity enzyme-linked immunosorbent assay (ELISA) method for measuring protein carbonyl in samples with low amounts of protein. Free Radic Biol Med 39: 1362–1367.
- Atkinson SD, Tuggle DW, Tunell WP. 1989. Hypoalbuminemia may predispose infants to necrotizing enterocolitis. J Pediatr Surg 24: 674–676.
- Ballmer PE, McNurlan MA, Essen P, Anderson SE, Garlick PJ. 1995. Albumin synthesis rates measured with [2H5ring]phenylalanine are not responsive to short-term intravenous nutrients in healthy humans. J Nutr 125: 512–519.
- Barker DJ, Eriksson JG, Forsen T, Osmond C. 2002. Fetal origins of adult disease: Strength of effects and biological basis. Int J Epidemiol 31: 1235–1239.
- Barle H, Nyberg B, Essen P, Andersson K, McNurlan MA, Wernerman J, Garlick PJ. 1997. The synthesis rates of total liver protein and plasma albumin determined simultaneously in vivo in humans. Hepatology 25: 154–158.
- Barle H, Hammarqvist F, Westman B, Klaude M, Rooyackers O, Garlick PJ, Wernerman J. 2006. Synthesis rates of total liver protein and albumin are both increased in patients with an acute inflammatory response. Clin Sci (Lond) 110: 93–99.
- Beylot M, David F, Brunengraber H. 1993. Determination of the 13C-labeling pattern of glutamate by gas chromatography-mass spectrometry. Anal Biochem 212: 532–536.
- Bier DM, Arnold KJ, Sherman WR, Holland WH, Holmes WF, Kipnis DM. 1977. In-vivo measurement of glucose and alanine metabolism with stable isotopic tracers. Diabetes 26: 1005–1015.
- Bjorkhem I, Blomstrand R, Falk O, Ohman G. 1976. The use of mass fragmentography in the evaluation of routine methods for glucose determination. Clin Chim Acta 72: 353–362.
- Blanc S, Colligan AS, Trabulsi J, Harris T, Everhart JE, Bauer D, Schoeller DA. 2002. Influence of delayed isotopic equilibration in urine on the accuracy of the (2)H(2)(18)O method in the elderly. J Appl Physiol 92: 1036–1044.
- Bohlin K, Patterson BW, Spence KL, Merchak A, Zozobrado JC, Zimmermann LJ, Carnielli VP, Hamvas A. 2005. Metabolic kinetics of pulmonary surfactant in newborn infants using endogenous stable isotope techniques. J Lipid Res 46: 1257–1265.
- Boschker HTS, Moerdijk-Poortvliet TCW, van Breugel P, Houtekamer M, Middelburg JJ. 2008. A versatile method for stable carbon isotope analysis of carbohydrates by high-performance liquid chromatography/isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 22: 3902–3908.
- Brenna JT, Corso TN, Tobias HJ, Caimi RJ. 1997. High-precision continuous-flow isotope ratio mass spectrometry. Mass Spectrom Rev 16: 227–258.
- Brown LD, Cheung A, Harwood JE, Battaglia FC. 2009. Inositol and mannose utilization rates in term and late-preterm infants exceed nutritional intakes. J Nutr 139: 1648–1652.
- Bunt JE, Rietveld T, Schierbeek H, Wattimena JL, Zimmermann LJ, van Goudoever JB. 2007. Albumin synthesis in preterm infants on the first day of life studied with [1-13C]leucine. Am J Physiol Gastrointest Liver Physiol 292: G1157–G1161.
- Cabanero AI, Recio JL, Ruperez M. 2006. Liquid chromatography coupled to isotope ratio mass spectrometry: A new perspective on honey adulteration detection. J Agric Food Chem 54: 9719–9727.
- Caimi RJ, Brenna JT. 1993. High-precision liquid chromatography-combustion isotope ratio mass spectrometry. Anal Chem 65: 3497–3500.
- Capitan P, Malmezat T, Breuille D, Obled C. 1999. Gas chromatographic-mass spectrometric analysis of stable isotopes of cysteine and glutathione in biological samples. J Chromatogr B Biomed Sci Appl 732: 127–135.
- Carnielli VP, Luijendijk IH, Van Goudoever JB, Sulkers EJ, Boerlage AA, Degenhart HJ, Sauer PJ. 1996. Structural position and amount of palmitic acid in infant formulas: Effects on fat, fatty acid, and mineral balance. J Pediatr Gastroenterol Nutr 23: 553–560.
- Caso G, Feiner J, Mileva I, Bryan LJ, Kelly P, Autio K, Gelato MC, McNurlan MA. 2007. Response of albumin synthesis to oral nutrients in young and elderly subjects. Am J Clin Nutr 85: 446–451.
- Chambrier C, Picard S, Vidal H, Cohen R, Riou JP, Beylot M. 1990. Interactions of glucagon and free fatty acids with insulin in control of glucose metabolism. Metabolism 39: 976–984.
- Chambrier C, Normand S, Ecochard R, Pachiaudi C, Laville M, Bouletreau P. 2001. Total-body-water measurement with (18)O-labeled water in short-bowel patients with an ileostomy. Nutrition 17: 287–291.
- Clapperton AT, Coward WA, Bluck LJ. 2002. Measurement of insulin sensitivity indices using 13C-glucose and gas chromatography/combustion/isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 16: 2009–2014.
- Clark SE, Karn CA, Ahlrichs JA, Wang J, Leitch CA, Leichty EA, Denne SC. 1997. Acute changes in leucine and phenylalanine kinetics produced by parenteral nutrition in premature infants. Pediatr Res 41: 568–574.
- Coplen TB, Brand WA, Gehre M, Groning M, Meijer HA, Toman B, Verkouteren RM. 2006. New guidelines for delta13C measurements. Anal Chem 78: 2439–2441.
- Cortiella J, Matthews DE, Hoerr RA, Bier DM, Young VR. 1988. Leucine kinetics at graded intakes in young men: Quantitative fate of dietary leucine. Am J Clin Nutr 48: 998–1009.
- Darmaun D, Smith SD, Sweeten S, Sager BK, Welch S, Mauras N. 2005. Evidence for accelerated rates of glutathione utilization and glutathione depletion in adolescents with poorly controlled type 1 diabetes. Diabetes 54: 190–196.
- de Bruin NC, Degenhart HJ, Gal S, Westerterp KR, Stijnen T, Visser HK. 1998. Energy utilization and growth in breast-fed and formula-fed infants measured prospectively during the first year of life. Am J Clin Nutr 67: 885–896.
- Debro JR, Korner A. 1956. Solubility of albumin in alcohol after precipitation by trichloroacetic acid: A simplified procedure for separation of albumin. Nature 178: 1067.
- Demmelmair H, Baumheuer M, Koletzko B, Dokoupil K, Kratl G. 2001. Investigation of long-chain polyunsaturated fatty acid metabolism in lactating women by means of stable isotope techniques. Adv Exp Med Biol 501: 169–1177.
- Desage M, Guilluy R, Brazier JL, Riou JP, Beylot M, Normand S, Vidal H. 1989. Positional isotopic analysis of 13C-labelled glucose by mass spectrometry: Applications to the study of gluconeogenesis in liver cells. Biomed Environ Mass Spectrom 18: 1010–1015.
- Dudley MA, Burrin DG, Wykes LJ, Toffolo G, Cobelli C, Nichols BL, Rosenberger J, Jahoor F, Reeds PJ. 1998. Protein kinetics determined in vivo with a multiple-tracer, single-sample protocol: Application to lactase synthesis. Am J Physiol 274: G591–G598.
- Ekberg K, Landau BR, Wajngot A, Chandramouli V, Efendic S, Brunengraber H, Wahren J. 1999. Contributions by kidney and liver to glucose production in the postabsorptive state and after 60 h of fasting. Diabetes 48: 292–298.
- Escobar J, Frank JW, Suryawan A, Nguyen HV, Davis TA. 2007. Amino acid availability and age affect the leucine stimulation of protein synthesis and eIF4F formation in muscle. Am J Physiol Endocrinol Metab 293: E1615–E1621.
- Faure M, Moennoz D, Montigon F, Mettraux C, Breuille D, Ballevre O. 2005. Dietary threonine restriction specifically reduces intestinal mucin synthesis in rats. J Nutr 135: 486–491.
- Faure M, Chone F, Mettraux C, Godin JP, Bechereau F, Vuichoud J, Papet I, Breuille D, Obled C. 2007. Threonine utilization for synthesis of acute phase proteins, intestinal proteins, and mucins is increased during sepsis in rats. J Nutr 137: 1802–1807.
- Fenn JB. 2002. Electrospray ionization mass spectrometry: How it all began. J Biomol Tech 13: 101–118.
- Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. 1989. Electrospray ionization for mass spectrometry of large biomolecules. Science 246: 64–71.
- Fjeld CR, Schoeller DA, Brown KH. 1989. A new model for predicting energy requirements of children during catch-up growth developed using doubly labeled water. Pediatr Res 25: 503–508.
- Gehre M, Strauch G. 2003. High-temperature elemental analysis and pyrolysis techniques for stable isotope analysis. Rapid Commun Mass Spectrom 17: 1497–1503.
- Gehre M, Geilmann H, Richter J, Werner RA, Brand WA. 2004. Continuous flow 2H/1H and 18O/16O analysis of water samples with dual inlet precision. Rapid Commun Mass Spectrom 18: 2650–2660.
- Giordano M, Castellino P, DeFronzo RA. 1996. Differential responsiveness of protein synthesis and degradation to amino acid availability in humans. Diabetes 45: 393–399.
- Godin JP, Hau J, Fay LB, Hopfgartner G. 2005. Isotope ratio monitoring of small molecules and macromolecules by liquid chromatography coupled to isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 19: 2689–2698.
- Godin JP, Fay LB, Hopfgartner G. 2007. Liquid chromatography combined with mass spectrometry for 13C isotopic analysis in life science research. Mass Spectrom Rev 26: 751–774.
- Godin JP, Breuille D, Obled C, Papet I, Schierbeek H, Hopfgartner G, Fay LB. 2008a. Liquid and gas chromatography coupled to isotope ratio mass spectrometry for the determination of 13C-valine isotopic ratios in complex biological samples. J Mass Spectrom 43: 1334–1343.
- Godin JP, Hopfgartner G, Fay L. 2008b. Temperature-programmed high-performance liquid chromatography coupled to isotope ratio mass spectrometry. Anal Chem 80: 7144–7152.
- Godin JP, Mermoud AF, Remond D, Faure M, Breuille D, Williamson G, Pere-Trepat E, Ramadan Z, Fay LB, Kochhar S. 2009. Simultaneous measurement of 13C- and 15N-isotopic enrichments of threonine by mass spectrometry. Rapid Commun Mass Spectrom 23: 1109–1115.
- Graham DY, Klein PD, Evans DJ Jr, Evans DG, Alpert LC, Opekun AR, Boutton TW. 1987. Campylobacter pylori detected noninvasively by the 13C-urea breath test. Lancet 1: 1174–1177.
- Guillet C, Boirie Y, Walrand S. 2004. An integrative approach to in-vivo protein synthesis measurement: From whole tissue to specific proteins. Curr Opin Clin Nutr Metab Care 7: 531–538.
- Guo ZK, Lee WN, Katz J, Bergner AE. 1992. Quantitation of positional isomers of deuterium-labeled glucose by gas chromatography/mass spectrometry. Anal Biochem 204: 273–282.
- Hallemeesch MM, Soeters PB, Deutz NE. 2000. Tracer methodology in whole body and organ balance metabolic studies: Plasma sampling is required. A study in post-absorptive rats using isotopically labeled arginine, phenylalanine, valine and leucine. Clin Nutr 19: 157–163.
- Heuer VEM, Tille S, Krummen M, Lollar XP, Hmelo LR, Hindrichs K. 2006. Online δ13C analysis of volatile fatty acids in sediment/porewater systems by liquid chromatography-isotope ratio-mass spectrometry. Limnol Oceangr Methods 4: 346–357.
- Huidekoper HH, Visser G, Ackermans MT, Sauerwein HP, Wijburg FA. 2010. A potential role for muscle in glucose homeostasis: In vivo kinetic studies in glycogen storage disease type 1a and fructose-1,6-bisphosphatase deficiency. J Inherit Metab Dis 33: 25–31.
- Iwata T, Iwata H, Holland JF. 1968. Isolation of albumin from human serum by means of trichloroacetic acid and ethanol. A comparison of methods. Clin Chem 14: 22–30.
- Jacobs R, Demmelmair H, Rittler P, Kellermann J, Koletzko B, Krick M, Jauch KW, Hartl WH. 2005. Isolation of plasma albumin by ethanol extraction is inappropriate for isotope ratio measurements during the acute phase response. J Chromatogr B Analyt Technol Biomed Life Sci 817: 145–151.
- Jahoor F, Wykes LJ, Reeds PJ, Henry JF, del Rosario MP, Frazer ME. 1995. Protein-deficient pigs cannot maintain reduced glutathione homeostasis when subjected to the stress of inflammation. J Nutr 125: 1462–1472.
- Jahoor F, Jackson A, Gazzard B, Philips G, Sharpstone D, Frazer ME, Heird W. 1999. Erythrocyte glutathione deficiency in symptom-free HIV infection is associated with decreased synthesis rate. Am J Physiol 276: E205–E211.
- Jaleel A, Nehra V, Persson XM, Boirie Y, Bigelow M, Nair KS. 2006. In vivo measurement of synthesis rate of multiple plasma proteins in humans. Am J Physiol Endocrinol Metab 291: E190–E197.
- Jansen G, Muskiet FA, Schierbeek H, Berger R, van der Slik W. 1986. Capillary gas chromatographic profiling of urinary, plasma and erythrocyte sugars and polyols as their trimethylsilyl derivatives, preceded by a simple and rapid prepurification method. Clin Chim Acta 157: 277–293.
- Kalhan SC, Bier DM, Savin SM, Adam PA. 1980. Estimation of glucose turnover and 13C recycling in the human newborn by simultaneous [1-13C]glucose and [6,6-1H2]glucose tracers. J Clin Endocrinol Metab 50: 456–460.
- Keijzer-Veen MG, Finken MJ, Nauta J, Dekker FW, Hille ET, Frolich M, Wit JM, van der Heijden AJ. 2005. Is blood pressure increased 19 years after intrauterine growth restriction and preterm birth? A prospective follow-up study in The Netherlands. Pediatrics 116: 725–731.
- Kien CL, Ault K, McClead RE. 1992. In vivo estimation of lactose hydrolysis in premature infants using a dual stable tracer technique. Am J Physiol 263: E1002–E1009.
- Kleger GR, Turgay M, Imoberdorf R, McNurlan MA, Garlick PJ, Ballmer PE. 2001. Acute metabolic acidosis decreases muscle protein synthesis but not albumin synthesis in humans. Am J Kidney Dis 38: 1199–1207.
- Koletzko B, Demmelmair H, Hartl W, Kindermann A, Koletzko S, Sauerwald T, Szitanyi P. 1998. The use of stable isotope techniques for nutritional and metabolic research in paediatrics. Early Hum Dev 53(Suppl): S77–S97.
- Koletzko B, Goulet O, Hunt J, Krohn K, Shamir R. 2005. Report on the guidelines on parenteral nutrition in infants, children and adolescents. Clin Nutr 24: 1105–1109.
-
Kornexl BE,
Gehre M,
Hofling R,
Werner RA.
1999.
On-line delta(18)O measurement of organic and inorganic substances.
Rapid Commun Mass Spectrom
13:
1685–1693.
10.1002/(SICI)1097-0231(19990830)13:16<1685::AID-RCM699>3.0.CO;2-9 CASPubMedWeb of Science®Google Scholar
- Krummen M, Hilkert AW, Juchelka D, Duhr A, Schluter HJ, Pesch R. 2004. A new concept for isotope ratio monitoring liquid chromatography/mass spectrometry. Rapid Commun Mass Spectrom 18: 2260–2266.
- Kury D, Keller U. 1991. Trimethylsilyl-O-methyloxime derivatives for the measurement of [6,6-2H2]-D-glucose-enriched plasma samples by gas chromatography-mass spectrometry. J Chromatogr 572: 302–306.
- Kuster A, Tea I, Sweeten S, Roze JC, Robins RJ, Darmaun D. 2008. Simultaneous determination of glutathione and cysteine concentrations and 2H enrichments in microvolumes of neonatal blood using gas chromatography-mass spectrometry. Anal Bioanal Chem 390: 1403–1412.
- Lavoie JC, Spalinger M, Chessex P. 1999. Glutathione synthetic activity in the lungs in newborn guinea pigs. Lung 177: 1–7.
- Law GK, Bertolo RF, Adjiri-Awere A, Pencharz PB, Ball RO. 2007. Adequate oral threonine is critical for mucin production and gut function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 292: G1293–G1301.
- Levine S. 1954. Solubilization of bovine albumin in nonaqueous media. Arch Biochem Biophys 50: 515–517.
- Liechty EA, Boyle DW, Moorehead H, Auble L, Denne SC. 1999. Aromatic amino acids are utilized and protein synthesis is stimulated during amino acid infusion in the ovine fetus. J Nutr 129: 1161–1166.
- Lifschitz CH, Boutton TW, Carrazza F, Beyreiss K, Schmitz J, Ricour C, Shulman R, Nichols BL. 1988. A carbon-13 breath test to characterize glucose absorption and utilization in children. J Pediatr Gastroenterol Nutr 7: 842–847.
- Lifson N, Little WS, Levitt DG, Henderson RM. 1975. D2 18O (deuterium oxide) method for CO2 output in small mammals and economic feasibility in man. J Appl Physiol 39: 657–664.
- Lucas A. 1998. Programming by early nutrition: An experimental approach. J Nutr 128: 401S–406S.
- Lucas A, Morley R, Cole TJ. 1998. Randomised trial of early diet in preterm babies and later intelligence quotient. BMJ 317: 1481–1487.
- Macdonald IA. 1999. Arterio-venous differences to study macronutrient metabolism: Introduction and overview. Proc Nutr Soc 58: 871–875.
- Magni F, Paroni R, Bonini PA, Kienle MG. 1992. Determination of serum glucose by isotope dilution mass spectrometry: Candidate definitive method. Clin Chem 38: 381–385.
- Matthews DE. 2007. An overview of phenylalanine and tyrosine kinetics in humans. J Nutr 137: 1549S–1555S; discussion 1573S–1575S.
- Matthews DE, Hayes JM. 1978. Isotope-ratio-monitoring gas chromatography-mass spectrometry. Anal Chem 11: 1465–1473.
- McCullagh JS, Juchelka D, Hedges RE. 2006. Analysis of amino acid 13C abundance from human and faunal bone collagen using liquid chromatography/isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 20: 2761–2768.
- McCullagh J, Gaye-Siessegger J, Focken U. 2008. Determination of underivatized amino acid delta(13)C by liquid chromatography/isotope ratio mass spectrometry for nutritional studies: The effect of dietary non-essential amino acid profile on the isotopic signature of individual amino acids in fish. Rapid Commun Mass Spectrom 22: 1817–1822.
- McFadden WH. 1976. Direct analysis of liquid chromatographic effluents. J Chromatogr 122. 389–396.
- McLean M, Vestal ML, Teffera Y, Abramson FP. 1996. Element- and isotope-specific detection for high-performance liquid chromatography using chemical reaction interface mass spectrometry. J Chromatogr A 732: 189–199.
- Meister A. 1991. Glutathione deficiency produced by inhibition of its synthesis, and its reversal; applications in research and therapy. Pharmacol Ther 51: 155–194.
- Michael SE. 1962. The isolation of albumin from blood serum or plasma by means of organic solvents. Biochem J 82: 212–218.
- Morris I, McCallion N, El-Khuffash A, Molloy EJ. 2008. Serum albumin and mortality in very low birth weight infants. Arch Dis Child Fetal Neonatal Ed 93: F310–F312.
- Orellana RA, O'Connor PM, Bush JA, Suryawan A, Thivierge MC, Nguyen HV, Fiorotto ML, Davis TA. 2006. Modulation of muscle protein synthesis by insulin is maintained during neonatal endotoxemia. Am J Physiol Endocrinol Metab 291: E159–E166.
- Paolini CL, Marconi AM, Pike AW, Fennessey PV, Pardi G, Battaglia FC. 2001. A multiple infusion start time (MIST) protocol for stable isotope studies of fetal blood. Placenta 22: 171–176.
- Parks EJ, Hellerstein MK. 2006. Thematic review series: Patient-oriented research. Recent advances in liver triacylglycerol and fatty acid metabolism using stable isotope labeling techniques. J Lipid Res 47: 1651–1660.
- Peters T Jr. 1996. All about albumin. Biochemistry, genetics, and medical applications. San Diego: Academic Press.
- Pickert A, Overkamp D, Renn W, Liebich H, Eggstein M. 1991. Selected ion monitoring gas chromatography/mass spectrometry using uniformly labelled (13C)glucose for determination of glucose turnover in man. Biol Mass Spectrom 20: 203–209.
- Poindexter BB, Karn CA, Ahlrichs JA, Wang J, Leitch CA, Liechty EA, Denne SC. 1997. Amino acids suppress proteolysis independent of insulin throughout the neonatal period. Am J Physiol 272: E592–E599.
- Poindexter BB, Karn CA, Leitch CA, Liechty EA, Denne SC. 2001. Amino acids do not suppress proteolysis in premature neonates. Am J Physiol Endocrinol Metab 281: E472–E478.
- Powrie JK, Smith GD, Hennessy TR, Shojaee-Moradie F, Kelly JM, Sonksen PH, Jones RH. 1992. Incomplete suppression of hepatic glucose production in non-insulin dependent diabetes mellitus measured with [6,6-2H2]glucose enriched glucose infusion during hyperinsulinaemic euglycaemic clamps. Eur J Clin Invest 22: 244–253.
- Pozler O, Neumann D, Vorisek V, Bukac J, Bures J, Kokstein Z. 2003. Development of gastric emptying in premature infants. Use of the (13)C-octanoic acid breath test. Nutrition 19: 593–596.
- Puiman PJ, Jensen M, Stoll B, Renes IB, de Bruijn AC, Dorst K, Schierbeek H, Schmidt M, Boehm G, Burrin DG, Sangild PT, van Goudoever JB. 2011. Intestinal threonine utilization for protein and mucin synthesis is decreased in formula-fed preterm pigs. J Nutr 141: 1306–1311.
- Pupim LB, Flakoll PJ, Ikizler TA. 2004. Nutritional supplementation acutely increases albumin fractional synthetic rate in chronic hemodialysis patients. J Am Soc Nephrol 15: 1920–1926.
- Reeve EB, Pearson JR, Martz DC. 1963. Plasma protein synthesis in the liver: Method for measurement of albumin formation in vivo. Science 139: 914–916.
- Reid M, Badaloo A, Forrester T, Morlese JF, Frazer M, Heird WC, Jahoor F. 2000. In vivo rates of erythrocyte glutathione synthesis in children with severe protein-energy malnutrition. Am J Physiol Endocrinol Metab 278: E405–E412.
- Remond D, Buffiere C, Godin JP, Mirand PP, Obled C, Papet I, Dardevet D, Williamson G, Breuille D, Faure M. 2009. Intestinal inflammation increases gastrointestinal threonine uptake and mucin synthesis in enterally fed minipigs. J Nutr 139: 720–726.
- Richelle M, Darimont C, Piguet-Welsch C, Fay LB. 2004. High-throughput simultaneous determination of plasma water deuterium and 18-oxygen enrichment using a high-temperature conversion elemental analyzer with isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 18: 795–798.
- Riedijk MA, van Goudoever JB. 2007. Splanchnic metabolism of ingested amino acids in neonates. Curr Opin Clin Nutr Metab Care 10: 58–62.
- Riedijk MA, Stoll B, Chacko S, Schierbeek H, Sunehag AL, van Goudoever JB, Burrin DG. 2007. Methionine transmethylation and transsulfuration in the piglet gastrointestinal tract. Proc Natl Acad Sci USA 104: 3408–3413.
- Rivera A Jr, Bell EF, Bier DM. 1993. Effect of intravenous amino acids on protein metabolism of preterm infants during the first three days of life. Pediatr Res 33: 106–111.
- Rojas-Escudero E, Alarcon-Jimenez AL, Elizalde-Galvan P, Rojo-Callejas F. 2004. Optimization of carbohydrate silylation for gas chromatography. J Chromatogr A 1027: 117–120.
- Rook D, Te Braake FW, Schierbeek H, Longini M, Buonocore G, van Goudoever JB. 2010. Glutathione synthesis rates in early postnatal life. Pediatr Res 67: 407–411.
- Sano M, Yotsui Y, Abe H, Sasaki S. 1976. A new technique for the detection of metabolites labelled by the isotope 13C using mass fragmentography. Biomed Mass Spectrom 3: 1–3.
- Schaart MW, Schierbeek H, van der Schoor SR, Stoll B, Burrin DG, Reeds PJ, van Goudoever JB. 2005. Threonine utilization is high in the intestine of piglets. J Nutr 135: 765–770.
- Schaart MW, Schierbeek H, de Bruijn AC, Tibboel D, van Goudoever JB, Renes IB. 2006. A novel method to determine small intestinal barrier function in human neonates in vivo. Gut 55: 1366–1367.
- Schaart MW, de Bruijn AC, Schierbeek H, Tibboel D, Renes IB, van Goudoever JB. 2009. Small intestinal MUC2 synthesis in human preterm infants. Am J Physiol Gastrointest Liver Physiol. 296: G1085–G1090.
- Schierbeek H, Berger R. 1989. Determination of succinylacetone and succinylacetoacetate in physiological samples as the common product 5(3)-methyl-3(5)-isoxazole propionic acid using an isotope dilution method and mass spectrometry. Clin Chim Acta 184: 243–250.
- Schierbeek H, Bijsterveld K, Chapman TE, van Luijk WH, Reijngoud DJ, Berger R. 1990a. Stable isotope dilution analysis of cystine in granulocyte suspensions as cysteine: A powerful method for the diagnosis, the follow-up, and treatment of patients with cystinosis. Clin Chim Acta 191: 39–47.
- Schierbeek H, Te Braake F, Godin JP, Fay LB, van Goudoever JB. 2007. Novel method for measurement of glutathione kinetics in neonates using liquid chromatography coupled to isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 21: 2805–2812.
- Schierbeek H, Moerdijk-Poortvliet TC, van den Akker CH, Te Braake FW, Boschker HT, van Goudoever JB. 2009a. Analysis of [U-(13)C(6)]glucose in human plasma using liquid chromatography/isotope ratio mass spectrometry compared with two other mass spectrometry techniques. Rapid Commun Mass Spectrom 23: 3824–3830.
- Schierbeek H, Rieken R, Dorst KY, Penning C, van Goudoever JB. 2009b. Validation of deuterium and oxygen18 in urine and saliva samples from children using on-line continuous-flow isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 23: 3549–3554.
- Schierbeek H, Rook D, te Braake FW, Dorst KY, Voortman G, Godin JP, Fay LB, van Goudoever JB. 2009c. Simultaneous analysis of (13)C-glutathione as its dimeric form GSSG and its precursor [1-(13)C]glycine using liquid chromatography/isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 23: 2897–2902.
- Schoeller DA. 1983. Energy expenditure from doubly labeled water: Some fundamental considerations in humans. Am J Clin Nutr 38: 999–1005.
- Schoeller DA. 1988. Measurement of energy expenditure in free-living humans by using doubly labeled water. J Nutr 118: 1278–1289.
- Schoeller DA, van Santen E, Peterson DW, Dietz W, Jaspan J, Klein PD. 1980. Total body water measurement in humans with 18O and 2H labeled water. Am J Clin Nutr 33: 2686–2693.
- Schoeller DA, Dietz W, van Santen E, Klein PD. 1982. Validation of saliva sampling for total body water determination by H2 18O dilution. Am J Clin Nutr 35: 591–594.
- Schoeller DA, Bandini LG, Levitsky LL, Dietz WH. 1988. Energy requirements of obese children and young adults. Proc Nutr Soc 47: 241–246.
- Scott RPW. 1974. Interface for on-line liquid chromatography—mass spectroscopy analysis. J Chromatogr 99. 395–405.
- Sekhar RV, McKay SV, Patel SG, Guthikonda AP, Reddy VT, Balasubramanyam A, Jahoor F. 2010. Glutathione synthesis is diminished in patients with uncontrolled diabetes and restored by dietary supplementation with cysteine and glycine. Diabetes Care. 34: 162–167.
- Slater C, Preston T, Weaver LT. 2001. Stable isotopes and the international system of units. Rapid Commun Mass Spectrom 15: 1270–1273.
- Smith CI, Fuller BT, Choy K, Richards MP. 2009. A three-phase liquid chromatographic method for delta13C analysis of amino acids from biological protein hydrolysates using liquid chromatography-isotope ratio mass spectrometry. Anal Biochem 390: 165–172.
- Speakman JR, Racey PA. 1988. The doubly-labelled water technique for measurement of energy expenditure in free-living animals. Sci Prog 72: 227–237.
- Tappy L, Acheson K, Curchod B, Schneiter P, Normand S, Pachiaudi C, Temler E, Riou JP, Jequier E. 1994. Overnight glucose metabolism in obese non-insulin-dependent diabetic patients and in healthy lean individuals. Clin Physiol 14: 251–265.
- Tayek JA, Bergner EA, Lee WP. 1991. Correction of glucose carbon recycling for the determination of ‘true’ hepatic glucose production rates by (1-13C1)glucose. Biol Mass Spectrom 20: 186–190.
- te Braake FWJ, Schierbeek H, de Groof K, Longini M, Buonocore G, van Goudoever JB. 2007. Glutathione kinetics and oxidative stress in pre term neonates in the first week of life. Acta Paediatr 96: 147–147.
- Te Braake FW, Schierbeek H, de Groof K, Vermes A, Longini M, Buonocore G, van Goudoever JB. 2008. Glutathione synthesis rates after amino acid administration directly after birth in preterm infants. Am J Clin Nutr 88: 333–339.
- Te Braake FW, Schierbeek H, Vermes A, Huijmans JG, van Goudoever JB. 2009. High-dose cysteine administration does not increase synthesis of the antioxidant glutathione preterm infants. Pediatrics 124: e978–e984.
- Tea I, Ferchaud-Roucher V, Kuster A, Darmaun D, Robins RJ. 2007. Determination of 13C isotopic enrichment of glutathione and glycine by gas chromatography/combustion/isotope ratio mass spectrometry after formation of the N- or N,S-ethoxycarbonyl methyl ester derivatives. Rapid Commun Mass Spectrom 21: 3245–3252.
- Teffera Y, Abramson FP, McLean M, Vestal M. 1993. Development of an isotope-selective high-performance liquid chromatography detector using chemical-reaction-interface mass spectrometry: Application to deuterated cortisol metabolites in urine. J Chromatogr 620: 89–96.
- Trowbridge FL, Graham GG, Wong WW, Mellits ED, Rabold JD, Lee LS, Cabrera MP, Klein PD. 1984. Body water measurements in premature and older infants using H2 18O isotopic determinations. Pediatr Res 18: 524–527.
- Tserng KY, Kalhan SC. 1983. Estimation of glucose carbon recycling and glucose turnover with [U-13C] glucose. Am J Physiol 245: E476–E482.
- Uauy R, Mena P, Rojas C. 2000. Essential fatty acids in early life: Structural and functional role. Proc Nutr Soc 59: 3–15.
- Van den Akker CH, Van Goudoever JB. 2010. Recent advances in our understanding of protein and amino acid metabolism in the human fetus. Curr Opin Clin Nutr Metab Care 13: 75–80.
- van den Akker CH, te Braake FW, Schierbeek H, Rietveld T, Wattimena DJ, Bunt JE, van Goudoever JB. 2007. Albumin synthesis in premature neonates is stimulated by parenterally administered amino acids during the first days of life. Am J Clin Nutr 86: 1003–1008.
- van den Akker CH, Schierbeek H, Rietveld T, Vermes A, Duvekot JJ, Steegers EA, van Goudoever JB. 2008. Human fetal albumin synthesis rates during different periods of gestation. Am J Clin Nutr 88: 997–1003.
- van den Akker CH, Schierbeek H, Dorst KY, Schoonderwaldt EM, Vermes A, Duvekot JJ, Steegers EA, van Goudoever JB. 2009. Human fetal amino acid metabolism at term gestation. Am J Clin Nutr 89: 153–160.
- van der Schoor SR, van Goudoever JB, Stoll B, Henry JF, Rosenberger JR, Burrin DG, Reeds PJ. 2001. The pattern of intestinal substrate oxidation is altered by protein restriction in pigs. Gastroenterology 121: 1167–1175.
- Van Der Schoor SR, Reeds PJ, Stoll B, Henry JF, Rosenberger JR, Burrin DG, Van Goudoever JB. 2002. The high metabolic cost of a functional gut. Gastroenterology 123: 1931–1940.
- van der Schoor SR, Stoll B, Wattimena DL, Buller HA, Tibboel D, Burrin DG, van Goudoever JB. 2004. Splanchnic bed metabolism of glucose in preterm neonates. Am J Clin Nutr 79: 831–837.
- van der Schoor SR, Schierbeek H, Bet PM, Vermeulen MJ, Lafeber HN, van Goudoever JB, van Elburg RM. 2010. Majority of dietary glutamine is utilized in first pass in preterm infants. Pediatr Res 67: 194–199.
- van der Schoor SR, Wattimena DL, Huijmans J, Vermes A, van Goudoever JB. 2007. The gut takes nearly all: Threonine kinetics in infants. Am J Clin Nutr 86: 1132–1138.
- van Dijk TH, Boer TS, Havinga R, Stellaard F, Kuipers F, Reijngoud DJ. 2003. Quantification of hepatic carbohydrate metabolism in conscious mice using serial blood and urine spots. Anal Biochem 322: 1–13.
-
Van Kreel BK,
Van der Vegt F,
Meers M,
Wagenmakers T,
Westerterp K,
Coward A.
1996.
Determination of total body water by a simple and rapid mass spectrometric method.
J Mass Spectrom
31:
108–111.
10.1002/(SICI)1096-9888(199601)31:1<108::AID-JMS279>3.0.CO;2-M CASPubMedWeb of Science®Google Scholar
- van Lingen RA, van Goudoever JB, Luijendijk IH, Wattimena JL, Sauer PJ. 1992. Effects of early amino acid administration during total parenteral nutrition on protein metabolism in pre-term infants. Clin Sci (Lond) 82: 199–203.
- van Marken Lichtenbelt WD, Westerterp KR, Wouters L. 1994. Deuterium dilution as a method for determining total body water: Effect of test protocol and sampling time. Br J Nutr 72: 491–497.
- van Meer H, van Straten EM, Baller JF, van Dijk TH, Plosch T, Kuipers F, Verkade HJ. 2010. The effects of intrauterine malnutrition on maternal-fetal cholesterol transport and fetal lipid synthesis in mice. Pediatr Res 68: 10–15.
- Verbruggen SC, Schierbeek H, Coss-Bu J, Joosten KF, Castillo L, van Goudoever JB. 2011. Albumin synthesis rates in post-surgical infants and septic adolescents; influence of amino acids, energy, and insulin. Clin Nutr. DOI: 10.1016/j.clu.2011.02.001.
- Visser GH, Boon PE, Meijer HA. 2000a. Validation of the doubly labeled water method in Japanese Quail Coturnix c. japonica chicks: Is there an effect of growth rate? J Comp Physiol [B] 170: 365–372.
- Visser GH, Dekinga A, Achterkamp B, Piersma T. 2000b. Ingested water equilibrates isotopically with the body water pool of a shorebird with unrivaled water fluxes. Am J Physiol Regul Integr Comp Physiol 279: R1795–R1804.
- Volpi E, Sheffield-Moore M, Rasmussen BB, Wolfe RR. 2001. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA 286: 1206–1212.
- Walrand S, Guillet C, Gachon P, Rousset P, Giraudet C, Vasson MP, Boirie Y. 2004. Protein synthesis rates of human PBMC and PMN can be determined simultaneously in vivo by using small blood samples. Am J Physiol Cell Physiol 286: C1474–C1478.
- Weerasooriya V, Rennie MJ, Anant S, Alpers DH, Patterson BW, Klein S. 2006. Dietary fiber decreases colonic epithelial cell proliferation and protein synthetic rates in human subjects. Am J Physiol Endocrinol Metab 290: E1104–E1108.
- Westerterp KR. 1998. Energy requirements assessed using the doubly-labelled water method. Br J Nutr 80: 217–218.
- Westerterp KR. 1999. Body composition, water turnover and energy turnover assessment with labelled water. Proc Nutr Soc 58: 945–951.
- White E, Welch VM, Sun T, Sniegoski LT, Schaffer R, Hertz HS, Cohen A. 1982. The accurate determination of serum glucose by isotope dilution mass spectrometry—Two methods. Biomed Mass Spectrom 9: 395–405.
- Wolfe RR. 1984. Tracers in metabolic research: Radioisotope and stable isotope/mass spectrometry methods. Lab Res Methods Biol Med 9: 1–287.
- Wolfe RR, Chinkes DL. 2004. Isotope tracers in metabolic research: Principles and practice of kinetic analysis. Hoboken, NJ: Wiley-Blackwell.
- Wolfe RR, Allsop JR, Burke JF. 1978. Fallibility of the intravenous glucose tolerance test as a measure of endogenous glucose turnover. Metabolism 27: 217–226.
- Wong WW, Lee LS, Klein PD. 1987. Deuterium and oxygen-18 measurements on microliter samples of urine, plasma, saliva, and human milk. Am J Clin Nutr 45: 905–913.
- Wykes LJ, Ball RO, Menendez CE, Ginther DM, Pencharz PB. 1992. Glycine, leucine, and phenylalanine flux in low-birth-weight infants during parenteral and enteral feeding. Am J Clin Nutr 55: 971–975.
- Yudkoff M, Nissim I, McNellis W, Polin R. 1987. Albumin synthesis in premature infants: Determination of turnover with [15N]glycine. Pediatr Res 21: 49–53.