Metabolic Response to Surgery in Infants and Children

Abstract

Considerable advances have been achieved in paediatric surgery during the last two decades, which can be partly ascribed to a better understanding of the physiological response to operations and the use of that knowledge to decrease the metabolic response where appropriate. Alongside this, minimally invasive surgery is now well established for many surgical conditions in the neonate, infant and child. The metabolic response to surgery differs in neonates to that seen in adults: there is a small increase in oxygen consumption and resting energy expenditure immediately after surgery with a return to normal levels by 12–24 h. The increase in resting energy expenditure is significantly greater in infants undergoing a major operation than in those subjected to a minor procedure. The limited increase in energy expenditure may be due to diversion of energy from growth to tissue repair. There are limited data available on older children, but they appear to have a different pattern of postoperative resting energy expenditure. There is a fall in the early postoperative period, similar to data collected in adults, but no late hypermetabolism. Protein metabolism mirrors energy expenditure and contributes to the overall changes observed. Various factors affect the magnitude of the response. It seems that in children intraoperative thermoregulation and metabolism are significant drivers of many of the postoperative changes. Minimally invasive surgery may maintain preoperative metabolic processes by altering the postoperative processes on a physiological level or by maintaining thermoregulation in children. The mechanism and potential benefit of these observations need further investigation.

energy metabolism - thermoregulation - laparoscopy - protein metabolism

References

• 1 Swyer PR. New perspectives in neonatal nutrition.  Biol Neonate. 1987;  52 ((Suppl 1)) 4-16
• 2 Wilmore DW. From Cuthbertson to fast-track surgery: 70 years of progress in reducing stress in surgical patients.  Ann Surg. 2002;  236 643-648
• 3 Kilger E, Weis F, Briegel J. et al . Stress doses of hydrocortisone reduce severe systemic inflammatory response syndrome and improve early outcome in a risk group of patients after cardiac surgery.  Crit Care Med. 2003;  31 1068-1074
• 4 Talmor M, Hydo L, Barie PS. Relationship of systemic inflammatory response syndrome to organ dysfunction, length of stay, and mortality in critical surgical illness: effect of intensive care unit resuscitation.  Arch Surg. 1999;  134 81-87
• 5 Anand KJ. The stress response to surgical trauma: from physiological basis to therapeutic implications.  Prog Food Nutr Sci. 1986;  10 67-132
• 6 Cheadle WG, Mercer-Jones M, Heinzelmann M. et al . Sepsis and septic complications in the surgical patient: who is at risk?.  Shock. 1996;  6 ((Suppl 1)) S6-S9
• 7 Mokart D, Capo C, Blache JL. et al . Early postoperative compensatory anti-inflammatory response syndrome is associated with septic complications after major surgical trauma in patients with cancer.  Br J Surg. 2002;  89 1450-1456
• 8 Muehlstedt SG, Lyte M, Rodriguez JL. Increased IL-10 production and HLA-DR suppression in the lungs of injured patients precede the development of nosocomial pneumonia.  Shock. 2002;  17 443-450
• 9 Yasukawa H, Ohishi M, Mori H. et al . IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages.  Nat Immunol. 2003;  4 551-556
• 10 Tilg H, Trehu E, Atkins MB. et al . Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55.  Blood. 1994;  83 113-118
• 11 Wiik H, Karttunen R, Haukipuro K. Maximal local and minimal systemic cytokine response to colorectal surgery: the influence of perioperative filgrastim.  Cytokine. 2001;  14 188-192
• 12 O’Nuallain EM, Puri P, Reen DJ. Early induction of IL-1 receptor antagonist (IL-1Ra) in infants and children undergoing surgery.  Clin Exp Immunol. 1993;  93 218-222
• 13 Bellon JM, Manzano L, Bernardos L. et al . Cytokine levels after open and laparoscopic cholecystectomy.  Eur Surg Res. 1997;  29 27-34
• 14 Baigrie RJ, Lamont PM, Kwiatkowski D. et al . Systemic cytokine response after major surgery.  Br J Surg. 1992;  79 757-760
• 15 Baigrie RJ, Lamont PM, Dallman M. et al . The release of interleukin-1 beta (IL-1) precedes that of interleukin 6 (IL-6) in patients undergoing major surgery.  Lymphokine Cytokine Res. 1991;  10 253-256
• 16 Duval EL, Kavelaars A, Veenhuizen L. et al . Pro- and anti-inflammatory cytokine patterns during and after cardiac surgery in young children.  Eur J Pediatr. 1999;  158 387-393
• 17 Tsukada K, Katoh H, Shiojima M. et al . Concentrations of cytokines in peritoneal fluid after abdominal surgery.  Eur J Surg. 1993;  159 475-479
• 18 Ertel W, Keel M, Bonaccio M. et al . Release of anti-inflammatory mediators after mechanical trauma correlates with severity of injury and clinical outcome.  J Trauma. 1995;  39 879-885
• 19 O’Nuallain EM, Puri P, Mealy K. et al . Induction of interleukin-1 receptor antagonist (IL-1ra) following surgery is associated with major trauma.  Clin Immunol Immunopathol. 1995;  76 96-101
• 20 Parry-Billings M, Baigrie RJ, Lamont PM. et al . Effects of major and minor surgery on plasma glutamine and cytokine levels.  Arch Surg. 1992;  127 1237-1240
• 21 Galle C, De MV, Motte S. et al . Early inflammatory response after elective abdominal aortic aneurysm repair: a comparison between endovascular procedure and conventional surgery.  J Vasc Surg. 2000;  32 234-246
• 22 Hansen TG, Tonnesen E, Andersen JB. et al . The peri-operative cytokine response in infants and young children following major surgery.  Eur J Anaesthesiol. 1998;  15 56-60
• 23 Chwals WJ, Fernandez ME, Jamie AC. et al . Relationship of metabolic indexes to postoperative mortality in surgical infants.  J Pediatr Surg. 1993;  28 819-822
• 24 Hall RI, Smith MS, Rocker G. The systemic inflammatory response to cardiopulmonary bypass: pathophysiological, therapeutic, and pharmacological considerations.  Anesth Analg. 1997;  85 766-782
• 25 Tokunaga A, Onda M, Fujita I. et al . Sequential changes in the cell mediators of peritoneal and wound fluids after surgery.  Surg Today. 1993;  23 841-844
• 26 Wiik H, Syrjala H, Karttunen R. et al . Neutrophil adhesion molecules in colorectal surgery: effect of filgrastim given perioperatively.  Eur J Surg. 2001;  167 700-704
• 27 van Berge Henegouwen M, van der Poll T, Deventer SJH. et al . Peritoneal cytokine release after elective gastrointestinal surgery and postoperative complications.  The American Journal of Surgery. 1998;  175 311-316
• 28 Akhtar K, Kamalky-asl ID, Lamb WR. et al . Metabolic and inflammatory responses after laparoscopic and open inguinal hernia repair.  Ann R Coll Surg Engl. 1998;  80 125-130
• 29 Cruickshank AM, Fraser WD, Burns HJ. et al . Response of serum interleukin-6 in patients undergoing elective surgery of varying severity.  Clin Sci (Lond). 1990;  79 161-165
• 30 Shenkin A, Fraser WD, Series J. et al . The serum interleukin 6 response to elective surgery.  Lymphokine Res. 1989;  8 123-127
• 31 Zieren J, Jacobi CA, Wenger FA. et al . Fundoplication: a model for immunologic aspects of laparoscopic and conventional surgery.  J Laparoendosc Adv Surg Tech A. 2000;  10 35-40
• 32 Jones MO, Pierro A, Hashim IA. et al . Postoperative changes in resting energy expenditure and interleukin 6 level in infants.  Br J Surg. 1994;  81 536-538
• 33 Bolke E, Jehle PM, Trautmann M. et al . Different acute-phase response in newborns and infants undergoing surgery.  Pediatr Res. 2002;  51 333-338
• 34 Bennett-Guerrero E, Panah MH, Barclay GR. et al . Decreased endotoxin immunity is associated with greater mortality and/or prolonged hospitalization after surgery.  Anesthesiology. 2001;  94 992-998
• 35 Berger D, Bolke E, Seidelmann M. et al . Time-scale of interleukin-6, myeloid related proteins (MRP), C reactive protein (CRP), and endotoxin plasma levels during the postoperative acute phase reaction.  Shock. 1997;  7 422-426
• 36 Tsang TM, Tam PK. Cytokine response of neonates to surgery.  J Pediatr Surg. 1994;  29 794-797
• 37 Klava A, Windsor AC, Farmery SM. et al . Interleukin-10.  A role in the development of postoperative immunosuppression. Arch Surg. 1997;  132 425-429
• 38 Kato M, Honda I, Suzuki H. et al . Interleukin-10 production during and after upper abdominal surgery.  Journal of Clinical Anesthesia. 1998;  10 184-188
• 39 Slotwinski R, Olszewski WL, Chaber A. et al . The soluble tumor necrosis factor receptor I is an early predictor of local infective complications after colorectal surgery.  J Clin Immunol. 2002;  22 289-296
• 40 Seghaye M, Duchateau J, Bruniaux J. et al . Interleukin-10 release related to cardiopulmonary bypass in infants undergoing cardiac operations.  J Thorac Cardiovasc Surg. 1996;  111 545-553
• 41 Pierro A. Metabolic response to neonatal surgery.  Curr Opin Pediatr. 1999;  11 230-236
• 42 Ward Platt MP, Tarbit MJ, Aynsley-Green A. The effects of anesthesia and surgery on metabolic homeostasis in infancy and childhood.  J Pediatr Surg. 1990;  25 472-478
• 43 Bellon JM, Manzano L, Larrad A. et al . Endocrine and immune response to injury after open and laparoscopic cholecystectomy.  Int Surg. 1998;  83 24-27
• 44 Thorell A, Efendic S, Gutniak M. et al . Insulin resistance after abdominal surgery.  Br J Surg. 1994;  81 59-63
• 45 Jones MO, Pierro A, Hammond P. et al . The effect of major operations on heart rate, respiratory rate, physical activity, temperature and respiratory gas exchange in infants.  Eur J Pediatr Surg. 1995;  5 9-12
• 46 Anand KJ, Hickey PR. Halothane-morphine compared with high-dose sufentanil for anesthesia and postoperative analgesia in neonatal cardiac surgery.  N Engl J Med. 1992;  326 1-9
• 47 Facchinetti F, Bagnoli F, Bracci R. et al . Plasma opioids in the first hours of life.  Pediatr Res. 1982;  16 95-98
• 48 Ljungqvist O, Thorell A, Gutniak M. et al . Glucose infusion instead of preoperative fasting reduces postoperative insulin resistance.  J Am Coll Surg. 1994;  178 329-336
• 49 Nygren J, Soop M, Thorell A. et al . Preoperative oral carbohydrate administration reduces postoperative insulin resistance.  Clin Nutr. 1998;  17 65-71
• 50 Sellden E. Peri-operative amino acid administration and the metabolic response to surgery.  Proc Nutr Soc. 2002;  61 337-343
• 51 Sellden E, Lindahl SG. Amino acid-induced thermogenesis reduces hypothermia during anesthesia and shortens hospital stay.  Anesth Analg. 1999;  89 1551-1556
• 52 Widman J, Hammarqvist F, Sellden E. Amino acid infusion induces thermogenesis and reduces blood loss during hip arthroplasty under spinal anesthesia.  Anesth Analg. 2002;  95 1757-1762 table of contents 
• 53 Anand KJ, Sippell WG, Aynsley-Green A. Randomised trial of fentanyl anaesthesia in preterm babies undergoing surgery: effects on the stress response.  Lancet. 1987;  1 62-66
• 54 Kehlet H. Manipulation of the metabolic response in clinical practice.  World J Surg. 2000;  24 690-695
• 55 Carli F, Webster J, Pearson M. et al . Protein metabolism after abdominal surgery: effect of 24-h extradural block with local anaesthetic.  Br J Anaesth. 1991;  67 729-734
• 56 Schricker T, Klubien K, Wykes L. et al . Effect of epidural blockade on protein, glucose, and lipid metabolism in the fasted state and during dextrose infusion in volunteers.  Anesthesiology. 2000;  92 62-69
• 57 Cuthbertson DP, Fell GS, Smith CM. et al . Metabolism after injury. I. Effects of severity, nutrition, and environmental temperature on protein potassium, zinc, and creatine.  Br J Surg. 1972;  59 926-931
• 58 Jones MO, Pierro A, Hammond P. et al . The metabolic response to operative stress in infants.  J Pediatr Surg. 1993;  28 1258-1262
• 59 Anand KJ, Aynsley-Green A. Measuring the severity of surgical stress in newborn infants.  J Pediatr Surg. 1988;  23 297-305
• 60 Chwals WJ, Letton RW, Jamie A. et al . Stratification of injury severity using energy expenditure response in surgical infants.  J Pediatr Surg. 1995;  30 1161-1164
• 61 McHoney M, Klein NJ, Eaton S. et al . Decreased monocyte class II MHC expression following major abdominal surgery in children is related to operative stress.  Pediatric Surgery International. 2006;  22 330-334
• 62 Forsberg E, Soop M, Thorne A. Energy expenditure and outcome in patients with multiple organ failure following abdominal surgery.  Intensive Care Med. 1991;  17 403-409
• 63 Ishizuka B, Kuribayashi Y, Kobayashi Y. et al . Stress responses during laparoscopy with CO2 insufflation and with mechanical elevation of the abdominal wall.  J Am Assoc Gynecol Laparosc. 2000;  7 363-371
• 64 Yoshida T, Kobayashi E, Suminaga Y. et al . Hormone-cytokine response. Pneumoperitoneum vs abdominal wall-lifting in laparoscopic cholecystectomy.  Surg Endosc. 1997;  11 907-910
• 65 Fukushima R, Kawamura YJ, Saito H. et al . Interleukin-6 and stress hormone responses after uncomplicated gasless laparoscopic-assisted and open sigmoid colectomy.  Dis Colon Rectum. 1996;  39 S29-S34
• 66 Nguyen NT, Goldman CD, Ho HS. et al . Systemic stress response after laparoscopic and open gastric bypass.  J Am Coll Surg. 2002;  194 557-566
• 67 Ordemann J, Jacobi CA, Schwenk W. et al . Cellular and humoral inflammatory response after laparoscopic and conventional colorectal resections.  Surg Endosc. 2001;  15 600-608
• 68 Schwenk W, Jacobi C, Mansmann U. et al . Inflammatory response after laparoscopic and conventional colorectal resections – results of a prospective randomized trial.  Langenbecks Arch Surg. 2000;  385 2-9
• 69 Wu FP, Sietses C, von Blomberg BM. et al . Systemic and peritoneal inflammatory response after laparoscopic or conventional colon resection in cancer patients: a prospective, randomized trial.  Dis Colon Rectum. 2003;  46 147-155
• 70 Torres A, Torres K, Paszkowski T. et al . Cytokine response in the postoperative period after surgical treatment of benign adnexal masses: comparison between laparoscopy and laparotomy.  Surgical Endoscopy and Other Interventional Techniques. 2007;  21 1841-1848
• 71 Hill AG, Connolly AB. Minimal access colonic surgery: Is it truly minimally invasive?.  Anz Journal of Surgery. 2006;  76 282-284
• 72 Yahara N, Abe T, Morita K. et al . Comparison of interleukin-6, interleukin-8, and granulocyte colony-stimulating factor production by the peritoneum in laparoscopic and open surgery.  Surgical Endoscopy and Other Interventional Techniques. 2002;  16 1615-1619
• 73 Wang LX, Qin WJ, Tian F. et al . Cytokine responses following laparoscopic or open pyeloplasty in children.  Surgical Endoscopy and Other Interventional Techniques. 2009;  23 544-549
• 74 McHoney M, Eaton S, Wade A. et al . Inflammatory response in children after laparoscopic vs open Nissen fundoplication: randomized controlled trial.  J Pediatr Surg. 2005;  40 908-913
• 75 Lyons B, Taylor A, Power C. et al . Postanaesthetic shivering in children.  Anaesthesia. 1996;  51 442-445
• 76 Brand MD, Chien LF, Ainscow EK. et al . The causes and functions of mitochondrial proton leak.  Biochim Biophys Acta. 1994;  1187 132-139
• 77 Dicker A, Ohlson KB, Johnson L. et al . Halothane selectively inhibits nonshivering thermogenesis.  Possible implications for thermoregulation during anesthesia of infants. Anesthesiology. 1995;  82 491-501
• 78 Plattner O, Semsroth M, Sessler DI. et al . Lack of nonshivering thermogenesis in infants anesthetized with fentanyl and propofol.  Anesthesiology. 1997;  86 772-777
• 79 Ohlson KB, Mohell N, Cannon B. et al . Thermogenesis in brown adipocytes is inhibited by volatile anesthetic agents.  A factor contributing to hypothermia in infants? Anesthesiology. 1994;  81 176-183
• 80 Zamparelli M, Eaton S, Quant PA. et al . Analgesic doses of fentanyl impair oxidative metabolism of neonatal hepatocytes.  J Pediatr Surg. 1999;  34 260-263
• 81 Cuthbertson DP, Smith CM, Tilstone WJ. The effect of transfer to a warm environment (30 degree C) on the metabolic response to injury.  Br J Surg. 1968;  55 513-516
• 82 Campbell RM, Cuthbertson DP. Effect of environmental temperature on the metabolic response to injury.  Q J Exp Physiol Cogn Med Sci. 1967;  52 114-129
• 83 McHoney M, Corizia L, Eaton S. et al . Laparoscopic surgery in children is associated with an intraoperative hypermetabolic response.  Surgical Endoscopy. 2006;  20 452-457
• 84 Holland AJ, Ford WD. The influence of laparoscopic surgery on perioperative heat loss in infants.  Pediatr Surg Int. 1998;  13 350-351
• 85 Carli F, Emery PW, Freemantle CA. Effect of peroperative normothermia on postoperative protein metabolism in elderly patients undergoing hip arthroplasty.  Br J Anaesth. 1989;  63 276-282
• 86 Taggart DP, McMillan DC, Preston T. et al . Effect of surgical injury and intraoperative hypothermia on whole body protein metabolism.  Am J Physiol. 1991;  260 E118-E125
• 87 Pierro A, Eaton S, Ong E. Neonatal physiology and metabolic considerations. In: Grosfeld JL, O’Neill JA, Fonkalsrud EW, Coran AG, editors. Pediatric Surgery. 6th ed. Philadelphia: Mosby Elsevier 2006 pp. 89-113
• 88 Pierro A, Carnielli V, Filler RM. et al . Partition of energy metabolism in the surgical newborn.  J Pediatr Surg. 1991;  26 581-586
• 89 Freymond D, Schutz Y, Decombaz J. et al . Energy balance, physical activity, and thermogenic effect of feeding in premature infants.  Pediatr Res. 1986;  20 638-645
• 90 Bodamer OA, Hoffmann GF, Visser GH. et al . Assessment of energy expenditure in metabolic disorders.  Eur J Pediatr. 1997;  156 ((Suppl 1)) S24-S28
• 91 Schutz Y, Rueda-Maza CM, Zaffanello M. et al . Whole-body protein turnover and resting energy expenditure in obese, prepubertal children.  Am J Clin Nutr. 1999;  69 857-862
• 92 Cuthbertson DP. Observations on the disturbance of metabolism produced by injury to the limbs.  Quart J Med. 1932;  25 233-246
• 93 Cuthbertson DP. Post-shock metabolic response.  Lancet. 1942;  239 433-437
• 94 Cuthbertson D. Intensive-care-metabolic response to injury.  Br J Surg. 1970;  57 718-721
• 95 Kinney JM, Dudrick SJ. Trauma workshop report: metabolic response to trauma, and nutrition.  J Trauma. 1970;  10 1065-1068
• 96 Kinney JM, Long CL, Gump FE. et al . Tissue composition of weight loss in surgical patients. I. Elective operation.  Ann Surg. 1968;  168 459-474
• 97 Long CL, Kopp K, Kinney JM. Energy demands during ambulation in surgical convalescence.  Surg Forum. 1969;  20 93-94
• 98 Jakob SM, Ensinger H, Takala J. Metabolic changes after cardiac surgery.  Curr Opin Clin Nutr Metab Care. 2001;  4 149-155
• 99 Luo K, Li JS, Li LT. et al . Operative stress response and energy metabolism after laparoscopic cholecystectomy compared to open surgery.  World J Gastroenterol. 2003;  9 847-850
• 100 Brandi LS, Bertolini R, Janni A. et al . Energy metabolism of thoracic surgical patients in the early postoperative period.  Effect of posture. Chest. 1996;  109 630-637
• 101 Hersio K, Takala J, Kari A. et al . Patterns of energy expenditure in intensive-care patients.  Nutrition. 1993;  9 127-132
• 102 Watters JM, March RJ, Desai D. et al . Epidural anaesthesia and analgesia do not affect energy expenditure after major abdominal surgery.  Can J Anaesth. 1993;  40 314-319
• 103 Sato N, Oyamatsu M, Tsukada K. et al . Serial changes in contribution of substrates to energy expenditure after transthoracic esophagectomy for cancer.  Nutrition. 1997;  13 100-103
• 104 Cuthbertson DP, Rahimi AG. Metabolism after injury. 2. Effect of a dryish and warm environment on skin temperatures and electrolyte responses.  Br J Surg. 1973;  60 421-428
• 105 Cuthbertson DP, Fell GS, Rahimi AG. et al . Environmental temperature and metabolic response to injury protein, mineral and energy metabolism.  Adv Exp Med Biol. 1972;  33 409-416
• 106 Kotani G, Usami M, Kasahara H. et al . The relationship of IL-6 to hormonal mediators, fuel utilization, and systemic hypermetabolism after surgical trauma.  Kobe J Med Sci. 1996;  42 187-205
• 107 Humberstone DA, Shaw JH. Isotopic studies during surgical convalescence.  Br J Surg. 1989;  76 154-158
• 108 Akasu K. Energy metabolism after cardiac surgery utilizing the indirect calorimeter: a new breath by breath technique.  Kurume Med J. 2000;  47 55-62
• 109 Chiara O, Giomarelli PP, Biagioli B. et al . Hypermetabolic response after hypothermic cardiopulmonary bypass.  Crit Care Med. 1987;  15 995-1000
• 110 Puhakka K, Rasanen J, Leijala M. et al . Oxygen consumption following pediatric cardiac surgery.  J Cardiothorac Vasc Anesth. 1994;  8 642-648
• 111 Li J, Schulze-Neick I, Lincoln C. et al . Oxygen consumption after cardiopulmonary bypass surgery in children: Determinants and implications.  J Thorac Cardiovasc Surg. 2000;  119 525-533
• 112 Gebara BM, Gelmini M, Sarnaik A. Oxygen consumption, energy expenditure, and substrate utilization after cardiac surgery in children.  Crit Care Med. 1992;  20 1550-1554
• 113 Mitchell IM, Davies PS, Day JM. et al . Energy expenditure in children with congenital heart disease, before and after cardiac surgery.  J Thorac Cardiovasc Surg. 1994;  107 374-380
• 114 Jones MO, Pierro A, Hammond P. et al . The metabolic response to operative stress in infants.  J Pediatr Surg. 1993;  28 1258-1262
• 115 Shanbhogue RL, Lloyd DA. Absence of hypermetabolism after operation in the newborn infant.  JPEN J Parenter Enteral Nutr. 1992;  16 333-336
• 116 Shanbhogue RL, Jackson M, Lloyd DA. Operation does not increase resting energy expenditure in the neonate.  J Pediatr Surg. 1991;  26 578-580
• 117 Anand KJS, Sippell WG, Aynsley-Green A. Randomised trial of fentanyl anaesthesia in preterm babies undergoing surgery: effects on the stress response.  Lancet. 1987;  1 62-66
• 118 Anand KJS, Sippell WG, Aynsley-Green A. Randomised trial of fentanyl anaesthesia in preterm babies undergoing surgery: effects on the stress response.  Lancet. 1987;  1 62-66
• 119 Anand KJS, Hickey PR. Halothane-morphine compared with high-dose sufentanil for anesthesia and postoperative analgesia in neonatal cardiac surgery.  N Engl J Med. 1992;  326 1-9
• 120 Facchinetti F, Bagnoli F, Bracci R. et al . Plasma opioids in the first hours of life.  Pediatr Res. 1982;  16 95-98
• 121 Powis MR, Smith K, Rennie M. et al . Effect of major abdominal operations on energy and protein metabolism in infants and children.  J Pediatr Surg. 1998;  33 49-53
• 122 Powis MR, Smith K, Rennie M. et al . Characteristics of protein and energy metabolism in neonates with necrotizing enterocolitis – a pilot study.  J Pediatr Surg. 1999;  34 5-10
• 123 Powis MR, Smith K, Rennie M. et al . Effect of major abdominal operations on energy and protein metabolism in infants and children.  J Pediatr Surg. 1998;  33 49-53
• 124 Groner JI, Brown MF, Stallings VA. et al . Resting energy expenditure in children following major operative procedures.  J Pediatr Surg. 1989;  24 825-827
• 125 Fellander G, Nordenstrom J, Tjader I. et al . Lipolysis during abdominal surgery.  J Clin Endocrinol Metab. 1994;  78 150-155
• 126 Carli F, Lattermann R, Schricker T. Epidural analgesia and postoperative lipid metabolism: stable isotope studies during a fasted/fed state.  Reg Anesth Pain Med. 2002;  27 132-138
• 127 Zerr KJ, Furnary AP, Grunkemeier GL. et al . Glucose control lowers the risk of wound infection in diabetics after open heart operations.  Ann Thorac Surg. 1997;  63 356-361
• 128 Carli F, Halliday D. Modulation of protein metabolism in the surgical patient. Effect of 48-hour continuous epidural block with local anesthetics on leucine kinetics.  Reg Anesth. 1996;  21 430-435
• 129 Clague MB, Keir MJ, Wright PD. et al . The effects of nutrition and trauma on whole-body protein metabolism in man.  Clin Sci (Lond). 1983;  65 165-175
• 130 Essen P, Thorell A, McNurlan MA. et al . Laparoscopic cholecystectomy does not prevent the postoperative protein catabolic response in muscle.  Ann Surg. 1995;  222 36-42
• 131 Schricker T, Lattermann R, Fiset P. et al . Integrated analysis of protein and glucose metabolism during surgery: effects of anesthesia.  J Appl Physiol. 2001;  91 2523-2530
• 132 Exner R, Weingartmann G, Eliasen MM. et al . Glutamine deficiency renders human monocytic cells more susceptible to specific apoptosis triggers.  Surgery. 2002;  131 75-80
• 133 Lattermann R, Carli F, Wykes L. et al . Epidural blockade modifies perioperative glucose production without affecting protein catabolism.  Anesthesiology. 2002;  97 374-381
• 134 Carli F, Ramachandra V, Gandy J. et al . Effect of general anaesthesia on whole body protein turnover in patients undergoing elective surgery.  Br J Anaesth. 1990;  65 373-379
• 135 Hammarqvist F, Westman B, Leijonmarck CE. et al . Decrease in muscle glutamine, ribosomes, and the nitrogen losses are similar after laparoscopic compared with open cholecystectomy during the immediate postoperative period.  Surgery. 1996;  119 417-423
• 136 Arslanian SA, Kalhan SC. Protein turnover during puberty in normal children.  Am J Physiol. 1996;  270 E79-E84
• 137 Carli F, Webster J, Pearson M. et al . Postoperative protein metabolism: effect of nursing elderly patients for 24 h after abdominal surgery in a thermoneutral environment.  Br J Anaesth. 1991;  66 292-299
• 138 Elwyn DH, Gump FE, Munro HN. et al . Changes in nitrogen balance of depleted patients with increasing infusions of glucose.  Am J Clin Nutr. 1979;  32 1597-1611

Correspondence