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The end-product method of measuring whole-body protein turnover: a review of published results and a comparison with those obtained by leucine infusion

Published online by Cambridge University Press:  08 March 2007

S. L. Duggleby
Affiliation:
MRC Epidemiology Resource Centre, Southampton General Hospital, Southampton 5022 5A, UK
J. C. Waterlow*
Affiliation:
Nutrition Unit, Department of Epidemiology and Population Health, London School of Hygiene & Tropical Medicine, Keppel Street, London C1E 7HT, UK
*
*Corresponding author:
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Abstract

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The present review summarizes the results of all published papers on whole-body protein turnover in man measured by [15N]glycine and the end-product method using both urea and ammonia. It begins with a short account of the underlying assumptions and the justification for the use of [15N]glycine. The results are then compared with those of a large sample of measurements by the ‘gold standard’ precursor method with continuous infusion of [13C]leucine. The pros and cons of the two methods are compared and it is suggested that there is a place for further work by the less invasive end-product method, particularly for population studies of the genetic, environmental and functional determinants of whole-body rates of protein synthesis.

Type
Review article
Copyright
Copyright © The Nutrition Society 2005

References

Acheson, KJ, Decombaz, J, Piguet-Welsch, C, Montigon, F, Decarli, B, Bartholdi, I & Fern, EB (1995) Energy, protein and substrate metabolism in simulated microgravity. Am J Physiol 269 R252R260.Google Scholar
Ang, B, Halliday, D & Powell-Tuck, J (1995) Whole-body protein-turnover in response to hyperinsulinemia in humans postabsorptively with [N-15] glycine as tracer. Am J Clin Nutr 61, 10621066.CrossRefGoogle ScholarPubMed
Äqvist, SEG (1951) Metabolic interrelationships among amino acids studies with isotopic nitrogen. Acta Med Scand 5, 10461064.CrossRefGoogle Scholar
Arnal, MA, Mosoni, L & Boirie, Y (1999) Protein pulse feeding improves protein retention in elderly women. Am J Clin Nutr 69, 12021208.CrossRefGoogle ScholarPubMed
Badaloo, A, Jackson, AA & Jahoor, F (1989) Whole body protein turnover and resting metabolic rate in homozygous sickle cell disease. Clin Sci (Lond) 77, 9397.CrossRefGoogle ScholarPubMed
Bettany, GEA, Ang, BC, Georgiannos, SN, Halliday, D & Powell-Tuck, J (1996) Bed rest decreases whole-body protein turnover in post-absorptive man. Clin Sci (Lond) 90, 7375.CrossRefGoogle ScholarPubMed
Bier, DM (1989) Intrinsically difficult problems: the kinetics of body proteins and amino acids in man. Diabetes Metab Rev 5, 111132.Google Scholar
Bier, DM & Matthews, DE (1982) Stable isotope methods for in vivo investigations. Fed Proc 41, 26792685.Google Scholar
Binnerts, A, Swart, GR, Wilson, JHP, Hoogerbrugge, N, Pols, HAP, Birkenhager, JC & Lamberts, SWJ (1992) The effect of growth hormone administration in growth hormone deficient adults on bone, protein, carbohydrate and lipid homeostasis, as well as on body composition. Clin Endocrinol (Oxf) 37, 7987.CrossRefGoogle Scholar
Bonau, RA, Ang, SD, Jeevanandam, M & Daly, JM (1984) High branched chain amino acid solutions: relationship of composition to efficacy. JPEN J Parenter Enteral Nutr 8, 622627.Google Scholar
Bos, C, Benamouzig, R, Bruhat, A, Roux, C, Mahe, S, Valensi, P, Gaudichon, C, Ferriere, F, Rautureau, J & Tome, D (2000) Short-term protein and energy supplementation activates nitrogen kinetics and accretion in poorly nourished elderly subjects. Am J Clin Nutr 71, 11291137.Google Scholar
Catzeflis, C, Schütz, Y, Micheli, JL, Welsch, C, Arnaud, MJ & Jéquier, E (1985) Whole body protein synthesis and energy expenditure in very low birth weight infants. Pediatr Res 19, 679687.CrossRefGoogle ScholarPubMed
Conway, JM, Thorp, JW, Stein, TP, Seale, JL & Rumpler, WV (1995) Decreased protein synthesis during dry saturation diving. Undersea Hyperb Med 22, 219227.Google ScholarPubMed
de Benoist, B, Jackson, AA, Hill, JS & Persaud, C (1985) Whole-body protein turnover in Jamaican women during normal pregnancy. Hum Nutr Clin Nutr 39, 167179.Google Scholar
Dietz, WH, Wolfe, MH & Wolfe, RB (1982) A method for the rapid determination of protein turnover. Metab Clin Exp 31, 749754.Google Scholar
Dresler, CM, Jeevanandam, M & Brennan, MF (1987) Metabolic efficacy of enteral feeding in cancer and non-cancer patients. Metabolism 36, 8288.CrossRefGoogle Scholar
Duggleby, SL (1999) Protein turnover and urea kinetics during pregnancy, maternal body composition and fetal growth. PhD Thesis, University of Southampton.Google Scholar
Duggleby, SL & Jackson, AA (2001) Relationship of maternal protein turnover and lean body mass during pregnancy and birth length. Clin Sci (Lond) 101, 6572.Google Scholar
Duggleby, SL & Jackson, AA (2002) Protein, amino acid and nitrogen metabolism during pregnancy: how might the mother meet the needs of her fetus. Curr Opin Clin Nutr Metab Care 5, 503509.CrossRefGoogle ScholarPubMed
Eastell, R, Simmons, PS, Colwell, A, Assiri, MA, Burritt, MF, Russell, RGG & Riggs, BL (1992) Nyctohemeral changes in bone turnover assessed by serum bone Gla-protein concentration and urinary deoxypyridinoline excretion: effects of growth and ageing. Clin Sci (Lond) 83, 375382.Google Scholar
Fearon, KC, Hansell, DT, Preston, T, Plumb, JA, Davies, J, Shapiro, D, Shenkin, A, Calman, KC & Burns, HJ (1988) Influence of whole body protein turnover rate on resting energy expenditure in patients with cancer. Cancer Res 48, 25902595.Google ScholarPubMed
Fern, EB & Garlick, PJ (1983) The rate of nitrogen metabolism in the whole body of man measured with [15 N]-glycine and uniformly labelled [15 N]-wheat. Hum Nutr Clin Nutr 37, 91107.Google Scholar
Fern, EB, Garlick, PJ, McNurlan, MA & Waterlow, JC (1981) The excretion of isotope in urea and ammonia for estimating protein turnover in man with [15 N]glycine. Clin Sci (Lond) 61, 217228.Google Scholar
Fern, EB, Garlick, PJ, Sheppard, HG & Fern, M (1984) The precision of measuring the rate of whole body nitrogen flux and protein synthesis in man with a single dose of [15 N]-glycine. Hum Nutr Clin Nutr 38C, 6373.Google Scholar
Fern, EB, Garlick, PJ & Waterlow, JC (1985 a) The concept of the single body pool of metabolic nitrogen in determining the rate of whole-body nitrogen turnover. Hum Nutr Clin Nutr 39, 8599.Google ScholarPubMed
Fern, EB, Garlick, PJ & Waterlow, JC (1985 b) Apparent compartmentation of body nitrogen in one human subject: its consequences in measuring the rate of whole-body synthesis with 15 N. Clin Sci (Lond) 68, 271282.CrossRefGoogle Scholar
Garlick, PJ & Fern, EB (1985) Whole body protein turnover: theoretical consideration. In Substrate and Energy Metabolism. [Garrow, JS and Halliday, D, editors]. London: John Libbey.Google Scholar
Gausseres, N, Catala, I, Mahe, S, Luengo, C, Bornet, F, Guy-Grand, B & Tome, D (1997) Whole-body protein turnover in humans fed a soy protein-rich vegetable diet. Eur J Clin Nutr 51, 308311.CrossRefGoogle ScholarPubMed
Glass, RE, Fern, EB & Garlick, PJ (1983) Whole-body protein turnover before and after resection of colorectal tumours. Clin Sci (Lond) 64, 101108.CrossRefGoogle ScholarPubMed
Glynn, MJ, Metzner, S, Halliday, D & Powell-Tuck, J (1987) Whole body protein metabolism in parenterally fed patients. Glucose versus fat as the predominant energy source. Clin Nutr 6, 9196.Google Scholar
Glynn, MJ, Powell-Tuck, J & Halliday, D (1988) Reproducibility of whole body protein turnover measurements in an ‘ideal’ metabolic subject. Eur J Clin Nutr 42, 273275.Google Scholar
Golden, BE & Golden, MH (1992) Effect of zinc on lean tissue synthesis during recovery from malnutrition. Eur J Clin Nutr 46, 697706.Google ScholarPubMed
Golden, MHN & Waterlow, JC (1977) Total protein synthesis in elderly people: a comparison of results with [15 N]glycine and [14 C]leucine. Clin Sci Mol Med 53, 277288.Google ScholarPubMed
Grove, G & Jackson, AA (1995) Measurements of protein turnover in normal men using the end-product method with oral [15 N]-glycine: comparison of single dose and intermittent dose regimes. Br J Nutr 74, 491507.CrossRefGoogle Scholar
Jackson, AA, Duggleby, SL & Grove, G (2000) Whole body protein turnover can be measured non-invasively in women using the end product method with ( 15 N) glycine to show changes with the menstrual cycle and pregnancy. Eur J Clin Nutr 54, 329336.Google Scholar
Jackson, AA & Golden, MHN (1980) [15 N]Glycine metabolism in normal man: the metabolic α-amino-nitrogen pool. Clin Sci (Lond) 58, 577582.CrossRefGoogle Scholar
Jackson, AA, Golden, MH, Byfield, R, Jahoor, F, Royes, J & Soutter, L (1983) Whole-body protein turnover and nitrogen balance in young children at intakes of protein and energy in the region of maintenance. Hum Nutr Clin Nutr 37, 433446.Google Scholar
Jackson, AA, Persaud, C, Badaloo, V & de Benoist, B (1987) Whole-body protein turnover in man determined in three hours with oral or intravenous 15 N-glycine and enrichment in urinary ammonia. Hum Nutr Clin Nutr 41, 263276.Google Scholar
Jackson, AA, Shaw, JC, Barber, A & Golden, MH (1981) Nitrogen metabolism in preterm infants fed human donor breast milk: the possible essentiality of glycine. Pediatr Res 15, 14541461.Google Scholar
Jackson, AA, Soares, MJ, Grove, G & Waterlow, JC (1997) Enrichment in urinary ammonia and urea with hourly oral doses of [15 N]glycine; evidence for a step function and a circadian rhythm in protein turnover. Clin Sci (Lond) 93, 265271.CrossRefGoogle Scholar
Jeevanandam, M, Brennan, MF, Horowitz, GD, Rose, D, Mihranian, MF, Daly, J & Lowry, SF (1985) Tracer priming in human protein studies with [15 N]glycine. Biochem Med 34, 214225.CrossRefGoogle ScholarPubMed
Jeevanandam, M, Horowitz, GD, Lowry, SF & Brennan, MF (1984) Cancer cachexia and protein metabolism. Lancet 1, 14231426.Google Scholar
Jeevanandam, M, Legaspi, A, Lowry, SF, Horowitz, GD & Brennan, MF (1988) Effect of total parenteral nutrition on whole body protein kinetics in cachetic patients with benign or malignant disease. JPEN J Parenter Enteral Nutr 12, 229236.CrossRefGoogle ScholarPubMed
Jeevanandam, M, Leland, D, Shamos, RF, Casano, SF & Schiller, WR (1991) Glucose infusion improves endogenous protein synthesis efficiency in multiple trauma victims. Metabolism 40, 11991206.CrossRefGoogle ScholarPubMed
Jeevanandam, M, Lowry, SF & Brennan, MF (1987) Effect of the route of nutrient administration on whole-body protein kinetics in man. Metabolism 36, 968973.Google Scholar
Jeevanandam, M, Lowry, SF & Horowitz, GD (1986) Influencing dietary intake on whole body protein kinetics in normal man. Clin Nutr 5, 4148.Google Scholar
Jeevanandam, M, Petersen, SR & Shamos, RF (1993) Protein and glucose fuel kinetics and hormonal changes in elderly trauma patients. Metabolism 42, 12551262.Google Scholar
Jeevanandam, M, Shamos, RF & Petersen, SR (1992) Substrate efficacy in early nutrition support of critically ill multiple trauma victims. JPEN J Parenter Enteral Nutr 16, 511520.CrossRefGoogle ScholarPubMed
Jeevanandam, M, Young, DH & Schiller, WR (1989) Endogenous protein-synthesis efficiency in trauma victims. Metabolism 38, 967973.CrossRefGoogle ScholarPubMed
Jeevanandam, M, Young, DH & Schiller, WR (1991) Obesity and the metabolic response to severe multiple trauma in man. J Clin Invest 87, 262269.CrossRefGoogle ScholarPubMed
Kien, CL & Camitta, BM (1983) Increased whole-body protein turnover in sick children with newly diagnosed leukaemia or lymphoma. Cancer Res 43, 55865592.Google Scholar
Kondrup, J, Nielsen, K & Juul, A (1997) Effect of long-term refeeding on protein metabolism in patients with cirrhosis of the liver. Br J Nutr 77, 197212.Google Scholar
Lieberman, SA, Butterfield, GE, Harrison, D & Hoffman, AR (1994) Anabolic effects of recombinant insulin-like growth factor-1 in cachectic patients with the acquired immunodeficiency syndrome. J Clin Endocrinol Metab 78, 404410.Google ScholarPubMed
Lowry, SF, Legaspi, A, Jeevanandam, M, Horowitz, GD, Albert, JD & Brennan, MF (1986) Body protein kinetics during perioperative intravenous nutritional support. Surg Gynecol Obstet 163, 303309.Google Scholar
Ma, EL & Jiang, ZM (1990) Determination of protein turnover changes in perioperative patients by the 15 N-glycine constant infusion method. Proc Chin Acad Med Sci Peking Union Med Coll 5, 97101.Google Scholar
McNurlan, MA, McHardy, KC, Broom, J, Milne, E, Fearns, LM, Reeds, PJ & Garlick, PJ (1987) The effect of indomethacin on the response of protein synthesis to feeding in rats and man. Clin Sci (Lond) 73, 6975.CrossRefGoogle ScholarPubMed
Maouyo, D, Sarfati, P, Guan, D, Morisset, J & Adelson, JN (1993) Circadian rhythm of exocrine pancreatic secretion in rats: major and minor cycles. Am J Physiol 264, G792G800.Google Scholar
Marchini, JS, Moreira, EAM, Moreira, MZ, Hiramatsu, T, de Oliveira, JED & Vannucchi, H (1996) Whole-body protein metabolism turnover in men on a high or low calorie rice and bean Brazilian diet. Nutr Res 16, 435441.CrossRefGoogle Scholar
Marckman, P, Sanstrom, B & Jesperson, J (1993) Dietary effects on circulation fluctuations in human blood coagulation factor VII and fibrinolysis. Atherosclerosis 101, 225234.Google Scholar
Matthews, DE, Conway, JM, Young, VR & Bier, DM (1981) Glycine nitrogen metabolism in man. Metabolism 30, 886893.CrossRefGoogle ScholarPubMed
Mihranian, MH, Daly, JM, Ang, SD, Jeevanandam, M & Brennan, MF (1983) Whole-body protein-turnover, synthesis, and catabolism in surgical patients receiving branched-chain amino-acid enriched solutions. Surg Forum 34, 8084.Google Scholar
Nissim, I, Yuskoff, M & Segal, S (1983) A model for determination of total body protein synthesis based upon compartmental analysis of the plasma [15 N]glycine decay curve. Metabolism 32, 646653.Google Scholar
Pacy, PJ, Price, GM, Halliday, D, Quevedo, MR & Millward, DJ (1994) Nitrogen homoeostasis in man: the diurnal responses of protein synthesis and degradation and amino acid oxidation to diets with increasing protein intakes. Clin Sci (Lond) 86, 103118.CrossRefGoogle ScholarPubMed
Pannemans, DLE, Halliday, D & Westerterp, KR (1995) Whole body protein turnover in elderly men and women: responses to two protein intakes. Am J Clin Nutr 61, 3338.Google Scholar
Pannemans, DLE, Wagenmakers, AJM, Westerterp, KR, Schaafsma, G & Halliday, D (1997) The effect of an increase of protein intake on whole-body protein turnover in elderly women is tracer dependent. J Nutr 127, 17881794.Google Scholar
Pencharz, PB, Clarke, R, Archibald, EH & Vaisman, N (1988) The effect of a weight-reducing diet on the nitrogen metabolism of obese adolescents. Can J Physiol Pharmacol 66, 14691474.Google Scholar
Pencharz, PB, Clarke, R, Papageorgiou, A & Farri, L (1989) A reappraisal of protein turnover values in neonates fed human milk or formula. Can J Physiol Pharmacol 67, 282286.Google Scholar
Petersen, SR, Holaday, NJ & Jeevanandam, M (1994) Enhancement of protein synthesis efficiency in parentally fed trauma victims by adjuvant recombinant human growth hormone. J Trauma 36, 726733.Google Scholar
Petersen, SR, Jeevanandam, M & Harrington, T (1993) Is the metabolic response to injury different with or without severe head injury? Significance of plasma glutamine levels. J Trauma 34, 653660.CrossRefGoogle ScholarPubMed
Picou, D, Taylor-Roberts, T (1969) The measurement of total protein synthesis and catabolism and nitrogen turnover in infants in different nutritional states and receiving different amounts of dietary protein. Clin Sci (Lond) 36, 283296.Google Scholar
Pitts, RF & Pilkington, LA (1966) The relation between plasma concentrations of glutamine and glycine and utilization of their nitrogen as sources of urinary ammonia. J Clin Invest 45, 8693.CrossRefGoogle ScholarPubMed
Powell-Tuck, J, Fern, EB, Garlick, PJ & Waterlow, JC (1984) The effect of surgical trauma and insulin on whole-body protein turnover in parenterally-fed undernourished patients. Hum Nutr Clin Nutr 38, 1122.Google Scholar
Powell-Tuck, J & Glynn, MJ (1985) The effect of insulin infusion on whole-body protein metabolism in patients with gastrointestinal disease fed parenterally. Hum Nutr Clin Nutr 39, 181191.Google Scholar
Preston, T, Fearon, KCH, McMillan, DC, Winstanley, FP, Slater, C, Shenkin, A & Carter, DC (1995) Effect of ibuprofen on the acute-phase response and protein metabolism in patients with cancer and weight loss. Br J Surg 82, 229234.CrossRefGoogle ScholarPubMed
Read, WWC, McLaren, DS & Tchalian, M (1971) Urinary excretion of nitrogen from 15 N-labelled amino acids in the malnourished and recovered child. 1. Glycine and lysine. Clin Sci (Lond) 40, 375380.Google Scholar
Read, WWC, McLaren, DS & Tchalian, M (1972) Urinary excretion of nitrogen from ( 15 N) valine, ( 15 N) leucine and ( 15 N) isoleucine in malnourished and recovered children. Clin Sci (Lond) 42, 139143.CrossRefGoogle ScholarPubMed
Reeds, PJ & Harris, CI (1981) Protein turnover in animals: man in his context. In Nitrogen Metabolism in Man, pp. 391408 [Waterlow, JC and Stephen, JML, editors]. London: Applied Science Publishers.Google Scholar
Richards, EW, Long, CL, Nelson, KM, Tohver, OK, Pinkston, JA, Navari, RM & Blakemore, WS (1993) Protein turnover in advanced lung cancer patients. Metabolism 42, 291296.Google Scholar
Robinson, SM, Jaccard, C, Persaud, C, Jackson, AA, Jequier, E & Schutz, Y (1990) Protein turnover and thermogenesis in response to high-protein and high-carbohydrate feeding in men. Am J Clin Nutr 52, 7280.CrossRefGoogle ScholarPubMed
Slevin, K, Jackson, AA & Waterlow, JC (1991) A model for the measurement of whole body protein turnover incorporating a protein pool with life-time kinetics. Proc R Soc Lond 243, 8192.Google Scholar
Soares, MJ, Piers, LS, Shetty, PS, Jackson, AA & Waterlow, JC (1994) Whole body protein turnover in chronically undernourished individuals. Clin Sci (Lond) 86, 441446.Google Scholar
Soares, MJ, Piers, LS, Shetty, PS, Robinson, S, Jackson, AA & Waterlow, JC (1991) Basal metabolic rate, body composition and whole body protein turnover in Indian men with different nutritional status. Clin Sci (Lond) 81, 419425.CrossRefGoogle Scholar
Sprinson, DB & Rittenberg, D (1949) The rate of interaction of the amino acids of the diet with the tissue proteins. J Biol Chem 180, 715726.Google Scholar
Stein, TP, Leskiw, MJ & Schluter, MD (1996) Diet and nitrogen metabolism during spaceflight on the shuttle. J Appl Physiol 81, 8297.CrossRefGoogle ScholarPubMed
Stein, TP, Nutinsky, D, Condoluce, D, Schluter, MD & Leskiw, MJ (1990) Protein and energy substrate metabolism in AIDS patients. Metabolism 39, 876881.Google Scholar
Stein, TP, Pumpler, WV, Leskiw, MJ, Schluter, MD, Staples, R & Bodwell, CE (1991) Effect of reduced dietary intake on energy expenditure, protein turnover, and glucose cycling in man. Metab Clin Exp 40, 478483.CrossRefGoogle ScholarPubMed
Stroud, MA, Jackson, AA & Waterlow, JC (1996) Protein turnover rates of two human subjects during an unassisted crossing of Antarctica. Br J Nutr 76, 165174.Google Scholar
Swart, GR, Van den Berg, JW, Wattimena, JL, Rietveld, T, Van Vuure, JK & Frenkel, M (1988) Elevated protein requirements in cirrhosis of the liver investigated by whole body protein turnover studies. Clin Sci (Lond) 75, 101107.Google Scholar
Taggart, DP, McMillan, DC, Preston, T, Shenkin, A, Wheatley, DJ & Burns, HJG (1991) Effect of surgical injury and intraoperative hypothermia on whole-body protein-metabolism. Am J Physiol 260, E118E125.Google ScholarPubMed
Taruvinga, M, Jackson, AA & Golden, MHN (1979) Comparison of 15 N-labelled glycine, aspartate, valine and leucine for measurement of whole-body protein turnover. Clin Sci (Lond) 57, 281283.Google Scholar
Tomkins, AM, Garlick, PJ, Schofield, WN & Waterlow, JC (1983) The combined effects of infection and malnutrition in children. Clin Sci (Lond) 65, 313324.Google Scholar
Tracey, KJ, Legaspi, A, Albert, JD, Jeevanandam, M, Matthews, DE, Brennan, MF & Lowry, SF (1988) Protein and substrate metabolism during starvation and parenteral refeeding. Clin Sci (Lond) 74, 123132.CrossRefGoogle ScholarPubMed
Vaisman, N, Clarke, R, Rossi, M, Goldberg, E, Zello, GA & Pencharz, PB (1992) Protein turnover and resting energy expenditure in patients with undernutrition and chronic lung disease. Am J Clin Nutr 55, 6369.Google Scholar
Vaisman, N, Stallings, VA, Chan, H, Weitzman, SS, Clarke, R & Pencharz, PB (1993) Effect of chemotherapy on the energy and protein-metabolism of children near the end of treatment for acute lymphoblastic-leukemia. Am J Clin Nutr 57, 679684.CrossRefGoogle ScholarPubMed
Van Goudoever, JB, Sulkers, EJ, Halliday, D, Degenhart, HJ, Carnielli, VP, Wattimena, JL & Sauer, PJ (1995) Whole-body protein turnover in preterm appropriate for gestational age and small for gestational age infants: comparison of [15 N]glycine and [1- 13 C]leucine administered simultaneously. Pediatr Res 37, 381388.Google Scholar
Waterlow, JC (In press) Protein Turnover in Man. Wallingford: CABI Publishing.Google Scholar
Waterlow, JC, Garlick, PJ & Millward, DJ (1978 a) Protein Turnover in Mammalian Tissues and in the Whole Body. Amsterdam: North-Holland.Google Scholar
Waterlow, JC, Golden, MHN & Garlick, PS (1978) Protein turnover in man measured with 15 N: comparison of end products and dose regimes. Am J Physiol 235, E165E174.Google Scholar
Watson, PE, Watson, TD & Ball, R (1980) Total body water volumes for adult males and females estimated from simple anthropometric measurements. Am J Clin Nutr 33, 2739.Google Scholar
Willommet, L, Schutz, Y, Whitehead, R, Jequier, E & Fern, EB (1992) Whole body protein metabolism and resting energy expenditure in pregnant Gambian women. Am J Physiol 263, E624E631.Google Scholar
Wolman, SI, Sheppard, H, Fern, M & Waterlow, JC (1985) The effect of tri-iodothyronine (T 3 ) on protein turnover and metabolic rate. Int J Obes 8, 459463.Google Scholar
Yoshida, S, Noake, T, Tanaka, Y, Ishibashi, N, Shirouzu, Y, Shirouzu, K, Kakegawat Stein, TP (1996) Effect of fentanyl citrate anesthesia on protein turnover in patients with esophagectomy. J Surg Res 64, 120127.Google Scholar
Zillikens, MC, Van den Berg, JW, Wattimena, JL, Rietveld, T & Swart, GR (1993) Nocturnal oral glucose supplementation. The effects on protein metabolism in cirrhotic patients and in healthy controls. J Hepatol 17, 377383.Google Scholar
Zilversmit, DB (1960) The design and analysis of isotope experiments. Am J Med 29, 832848.Google Scholar