New insights into the controversy of adrenal function during critical illness

The Lancet Diabetes and Endocrinology

Volumn 3, Issue 10, 2015, Pages 805-815

  Boonen, Eva ^a   Bornstein, Stefan R ^b,c   Van den Berghe, Greet ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^b UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MELANOCORTIN 2 RECEPTOR; TRANSCORTIN;

ACUTE STRESS; ADRENAL CELL; ADRENAL CORTEX FUNCTION; ADRENAL INSUFFICIENCY; CHROMAFFIN CELL; CHRONIC STRESS; CORTICOSTEROID METABOLISM; CRITICALLY ILL PATIENT; HORMONE SYNTHESIS; HOSPITAL ADMISSION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INTENSIVE CARE UNIT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STEROIDOGENESIS; SYSTEMATIC REVIEW (TOPIC); SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; ADRENAL CORTEX; ADRENAL GLAND; CRITICAL ILLNESS; FEEDBACK SYSTEM; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM;

ADRENAL CORTEX; ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; CRITICAL ILLNESS; FEEDBACK, PHYSIOLOGICAL; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM;

EID: 84941801646     PISSN: 22138587     EISSN: 22138595     Source Type: Journal    
DOI: 10.1016/S2213-8587(15)00224-7     Document Type: Review

References (83)

1. Chrousos GP, Gold PW The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 1992, 267:1244-1252.
2. Bornstein SR, Briegel J A new role for glucocorticoids in septic shock: balancing the immune response. Am J Respir Crit Care Med 2003, 167:485-486.
3. Galon J, Franchimont D, Hiroi N, et al. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J 2002, 16:61-71.
4. Annane D, Maxime V, Ibrahim F, Alvarez JC, Abe E, Boudou P Diagnosis of adrenal insufficiency in severe sepsis and septic shock. Am J Respir Crit Care Med 2006, 174:1319-1326.
5. Lebrethon MC, Naville D, Begeot M, Saez JM Regulation of corticotropin receptor number and messenger RNA in cultured human adrenocortical cells by corticotropin and angiotensin II. J Clin Invest 1994, 93:1828-1833.
6. Lehoux JG, Lefebvre A, Bélisle S, Bellabarba D Hormonal regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase mRNA in the rat adrenal gland. J Steroid Biochem 1989, 34:379-384.
7. Lehoux JG, Fleury A, Ducharme L The acute and chronic effects of adrenocorticotropin on the levels of messenger ribonucleic acid and protein of steroidogenic enzymes in rat adrenal in vivo. Endocrinology 1998, 139:3913-3922.
8. Liu J, Heikkilä P, Meng QH, Kahri AI, Tikkanen MJ, Voutilainen R Expression of low and high density lipoprotein receptor genes in human adrenals. Eur J Endocrinol 2000, 142:677-682.
9. Simpson ER, Waterman MR Regulation by ACTH of steroid hormone biosynthesis in the adrenal cortex. Can J Biochem Cell Biol 1983, 61:692-707.
10. Stocco DM, Clark BJ Regulation of the acute production of steroids in steroidogenic cells. Endocr Rev 1996, 17:221-244.
11. Kanczkowskia W, Suea M, Zacharowskib K, Reinckec M, Bornstein SR The role of adrenal gland microenvironment in the HPA axis function and dysfunction during sepsis. Mol Cell Endocrinol 2014, published online Dec 24.
12. Chrousos GP The role of stress and the hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndrome: neuro-endocrine and target tissue-related causes. Int J Obes Relat Metab Disord 2000, 24(suppl 2):s50-s55.
13. Bornstein SR Predisposing factors for adrenal insufficiency. N Engl J Med 2009, 360:2328-2339.
14. Naito Y, Fukata J, Tamai S, et al. Biphasic changes in hypothalamo-pituitary-adrenal function during the early recovery period after major abdominal surgery. J Clin Endocrinol Metab 1991, 73:111-117.
15. Udelsman R, Norton JA, Jelenich SE, et al. Responses of the hypothalamic-pituitary-adrenal and renin-angiotensin axes and the sympathetic system during controlled surgical and anesthetic stress. J Clin Endocrinol Metab 1987, 64:986-994.
16. Ehrhart-Bornstein M, Hinson JP, Bornstein SR, Scherbaum WA, Vinson GP Intraadrenal interactions in the regulation of adrenocortical steroidogenesis. Endocr Rev 1998, 19:101-143.
17. Waterhouse R A case of suprarenal apoplexy. Lancet 1911, 1:577-578.
18. Bornstein SR, Ehrhart-Bornstein M, Güse-Behling H, Scherbaum WA Structure and dynamics of adrenal mitochondria following stimulation with corticotropin releasing hormone. Anat Rec 1992, 234:255-262.
19. Prasad R, Kowalczyk JC, Meimaridou E, Storr HL, Metherell LA Oxidative stress and adrenocortical insufficiency. J Endocrinol 2014, 221:R63-R73.
20. Szigethy E, Conwell Y, Forbes NT, Cox C, Caine ED Adrenal weight and morphology in victims of completed suicide. Biol Psychiatry 1994, 36:374-380.
21. Dinan T Novel approaches to the treatment of depression by modulating the hypothalamic-pituitary-adrenal axis. Hum Pscychopharmacol 2001, 16:89-93.
22. Lamounier-Zepter V, Ehrhart-Bornstein M, Bornstein SR Metabolic syndrome and the endocrine stress system. Horm Metab Res 2006, 38:437-441.
23. Drucker D, Shandling M Variable adrenocortical function in acute medical illness. Crit Care Med 1985, 13:477-479.
24. Michalaki M, Margeli T, Tsekouras A, Gogos CH, Vagenakis AG, Kyriazopoulou V Hypothalamic-pituitary-adrenal axis response to the severity of illness in non-critically ill patients: does relative corticosteroid insufficiency exist?. Eur J Endocrinol 2010, 162:341-347.
25. Roth-Isigkeit AK, Schmucker P Postoperative dissociation of blood levels of cortisol and adrenocorticotropin after coronary artery bypass grafting surgery. Steroids 1997, 62:695-699.
26. Vermes I, Beishuizen A, Hampsink RM, Haanen C Dissociation of plasma adrenocorticotropin and cortisol levels in critically ill patients: possible role of endothelin and atrial natriuretic hormone. J Clin Endocrinol Metab 1995, 80:1238-1242.
27. Boonen E, Vervenne H, Meersseman P, et al. Reduced cortisol metabolism during critical illness. N Engl J Med 2013, 368:1477-1488.
28. Vassiliadi DA, Dimopoulou I, Tzanela M, et al. Longitudinal assessment of adrenal function in the early and prolonged phases of critical illness in septic patients: relations to cytokine levels and outcome. J Clin Endocrinol Metab 2014, 99:4471-4480.
29. Polito A, Sonneville R, Guidoux C, et al. Changes in CRH and ACTH synthesis during experimental and human septic shock. PLoS One 2011, 6:e25905.
30. Deutschman CS, Raj NR, McGuire EO, Kelz MB Orexinergic activity modulates altered vital signs and pituitary hormone secretion in experimental sepsis. Crit Care Med 2013, 41:e368-e375.
31. Gibbison B, Angelini GD, Lightman SL Dynamic output and control of the hypothalamic-pituitary-adrenal axis in critical illness and major surgery. Br J Anaesth 2013, 111:347-360.
32. Boonen E, Meersseman P, Vervenne H, et al. Reduced nocturnal ACTH-driven cortisol secretion during critical illness. Am J Physiol Endocrinol Metab 2014, 306:E883-E892.
33. Boonen E, Langouche L, Janssens T, et al. Impact of duration of critical illness on the adrenal glands of human intensive care patients. J Clin Endocrinol Metab 2014, 99:4214-4222.
34. Bornstein SR, Chrousos GP Clinical review 104: Adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: neural and immune inputs. J Clin Endocrinol Metab 1999, 84:1729-1736.
35. Bornstein SR, Engeland WC, Ehrhart-Bornstein M, Herman JP Dissociation of ACTH and glucocorticoids. Trends Endocrinol Metab 2008, 19:175-180.
36. Bornstein SR, Ehrhart M, Scherbaum WA, Pfeiffer EF Adrenocortical atrophy of hypophysectomized rats can be reduced by corticotropin-releasing hormone (CRH). Cell Tissue Res 1990, 260:161-166.
37. Bornstein SR, Ehrhart-Bornstein M, Scherbaum WA, Pfeiffer EF, Holst JJ Effects of splanchnic nerve stimulation on the adrenal cortex may be mediated by chromaffin cells in a paracrine manner. Endocrinology 1990, 127:900-906.
38. Engeland WC, Arnhold MM Neural circuitry in the regulation of adrenal corticosterone rhythmicity. Endocrine 2005, 28:325-332.
39. Bornstein SR, Breidert M, Ehrhart-Bornstein M, Kloos B, Scherbaum WA Plasma catecholamines in patients with Addison's disease. Clin Endocrinol (Oxf) 1995, 42:215-218.
40. Merke DP, Chrousos GP, Eisenhofer G, et al. Adrenomedullary dysplasia and hypofunction in patients with classic 21-hydroxylase deficiency. N Engl J Med 2000, 343:1362-1368.
41. Bornstein SR, Tian H, Haidan A, et al. Deletion of tyrosine hydroxylase gene reveals functional interdependence of adrenocortical and chromaffin cell system in vivo. Proc Natl Acad Sci USA 2000, 97:14742-14747.
42. Carroll BJ, Iranmanesh A, Keenan DM, Cassidy F, Wilson WH, Veldhuis JD Pathophysiology of hypercortisolism in depression: pituitary and adrenal responses to low glucocorticoid feedback. Acta Psychiatr Scand 2012, 125:478-491.
43. Petrowski K, Wintermann GB, Kirschbaum C, Bornstein SR Dissociation between ACTH and cortisol response in DEX-CRH test in patients with panic disorder. Psychoneuroendocrinology 2012, 37:1199-1208.
44. Franchimont D, Bouma G, Galon J, et al. Adrenal cortical activation in murine colitis. Gastroenterology 2000, 119:1560-1568.
45. Bornstein SR, Zacharowski P, Schumann RR, et al. Impaired adrenal stress response in toll-like receptor 2-deficient mice. Proc Natl Acad Sci USA 2004, 101:16695-16700.
46. Kanczkowski W, Alexaki VI, Tran N, et al. Hypothalamo-pituitary and immune-dependent adrenal regulation during systemic inflammation. Proc Natl Acad Sci USA 2013, 110:14801-14806.
47. Krug AW, Vleugels K, Schinner S, et al. Human adipocytes induce an ERK1/2 MAP kinases-mediated upregulation of steroidogenic acute regulatory protein (StAR) and an angiotensin II-sensitization in human adrenocortical cells. Int J Obes (Lond) 2007, 31:1605-1616.
48. Ansurudeen I, Willenberg HS, Kopprasch S, Krug AW, Ehrhart-Bornstein M, Bornstein SR Endothelial factors mediate aldosterone release via PKA-independent pathways. Mol Cell Endocrinol 2009, 300:66-70.
49. Ehrhart-Bornstein M, Lamounier-Zepter V, Schraven A, et al. Human adipocytes secrete mineralocorticoid-releasing factors. Proc Natl Acad Sci USA 2003, 100:14211-14216.
50. Yehuda R Status of glucocorticoid alterations in post-traumatic stress disorder. Ann N Y Acad Sci 2009, 1179:56-69.
51. Boyar RM, Hellman LD, Roffwarg H, et al. Cortisol secretion and metabolism in anorexia nervosa. N Engl J Med 1977, 296:190-193.
52. Römer B, Lewicka S, Kopf D, et al. Cortisol metabolism in depressed patients and healthy controls. Neuroendocrinology 2009, 90:301-306.
53. Veldhuis JD, Keenan DM, Pincus SM Motivations and methods for analyzing pulsatile hormone secretion. Endocr Rev 2008, 29:823-864.
54. Voerman HJ, Strack van Schijndel RJ, Groeneveld AB, de Boer H, Nauta JP, Thijs LG Pulsatile hormone secretion during severe sepsis: accuracy of different blood sampling regimens. Metabolism 1992, 41:934-940.
55. Beishuizen A, Thijs LG, Vermes I Patterns of corticosteroid-binding globulin and the free cortisol index during septic shock and multitrauma. Intensive Care Med 2001, 27:1584-1591.
56. Nguyen PT, Lewis JG, Sneyd J, Lee RS, Torpy DJ, Shorten PR Development of a formula for estimating plasma free cortisol concentration from a measured total cortisol concentration when elastase-cleaved and intact corticosteroid binding globulin coexist. J Steroid Biochem Mol Biol 2014, 141:16-25.
57. Vanhorebeek I, Peeters RP, Vander Perre S, et al. Cortisol response to critical illness: effect of intensive insulin therapy. J Clin Endocrinol Metab 2006, 91:3803-3813.
58. Chan WL, Carrell RW, Zhou A, Read RJ How changes in affinity of corticosteroid-binding globulin modulate free cortisol concentration. J Clin Endocrinol Metab 2013, 98:3315-3322.
59. Ho JT, Al-Musalhi H, Chapman MJ, et al. Septic shock and sepsis: a comparison of total and free plasma cortisol levels. J Clin Endocrinol Metab 2006, 91:105-114.
60. Estrada-Y-Martin RM, Orlander PR Salivary cortisol can replace free serum cortisol measurements in patients with septic shock. Chest 2011, 140:1216-1222.
61. Bergquist M, Nurkkala M, Rylander C, Kristiansson E, Hedenstierna G, Lindholm C Expression of the glucocorticoid receptor is decreased in experimental Staphylococcus aureus sepsis. J Infect 2013, 67:574-583.
62. Guerrero J, Gatica HA, Rodríguez M, Estay R, Goecke IA Septic serum induces glucocorticoid resistance and modifies the expression of glucocorticoid isoforms receptors: a prospective cohort study and in vitro experimental assay. Crit Care 2013, 17:R107.
63. Indyk JA, Candido-Vitto C, Wolf IM, et al. Reduced glucocorticoid receptor protein expression in children with critical illness. Horm Res Paediatr 2013, 79:169-178.
64. Ledderose C, Möhnle P, Limbeck E, et al. Corticosteroid resistance in sepsis is influenced by microRNA-124-induced downregulation of glucocorticoid receptor-α. Crit Care Med 2012, 40:2745-2753.
65. Meduri GU, Muthiah MP, Carratu P, Eltorky M, Chrousos GP Nuclear factor-kappaB- and glucocorticoid receptor alpha-mediated mechanisms in the regulation of systemic and pulmonary inflammation during sepsis and acute respiratory distress syndrome. Evidence for inflammation-induced target tissue resistance to glucocorticoids. Neuroimmunomodulation 2005, 12:321-338.
66. Peeters RP, Hagendorf A, Vanhorebeek I, et al. Tissue mRNA expression of the glucocorticoid receptor and its splice variants in fatal critical illness. Clin Endocrinol (Oxf) 2009, 71:145-153.
67. Siebig S, Meinel A, Rogler G, et al. Decreased cytosolic glucocorticoid receptor levels in critically ill patients. Anaesth Intensive Care 2010, 38:133-140.
68. van den Akker EL, Koper JW, Joosten K, et al. Glucocorticoid receptor mRNA levels are selectively decreased in neutrophils of children with sepsis. Intensive Care Med 2009, 35:1247-1254.
69. Krone N, Stewart PM Adrenal function: an overlooked cause of glucocorticoid deficiency?. Nat Rev Endocrinol 2009, 5:362-363.
70. Theocharidou E, Krag A, Bendtsen F, Møller S, Burroughs AK Cardiac dysfunction in cirrhosis-does adrenal function play a role? A hypothesis. Liver Int 2012, 32:1327-1332.
71. Selye H The general adaptation syndrome and the diseases of adaptation. J Clin Endocrinol Metab 1946, 6:117-230.
72. Annane D, Sébille V, Troché G, Raphaël JC, Gajdos P, Bellissant E A 3-level prognostic classification in septic shock based on cortisol levels and cortisol response to corticotropin. JAMA 2000, 283:1038-1045.
73. Marik PE, Pastores SM, Annane D, et al. Recommendations for the diagnosis and management of corticosteroid insufficiency in critically ill adult patients: consensus statements from an international task force by the American College of Critical Care Medicine. Crit Care Med 2008, 36:1937-1949. the American College of Critical Care Medicine.
74. Marik PE Critical illness-related corticosteroid insufficiency. Chest 2009, 135:181-193.
75. Charmandari E, Nicolaides NC, Chrousos GP Adrenal insufficiency. Lancet 2014, 383:2152-2167.
76. van der Voort PH, Gerritsen RT, Bakker AJ, Boerma EC, Kuiper MA, de Heide L HDL-cholesterol level and cortisol response to synacthen in critically ill patients. Intensive Care Med 2003, 29:2199-2203.
77. Dellinger RP, Levy MM, Carlet JM, et al. Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med 2008, 36:296-327. the International Surviving Sepsis Campaign Guidelines Committee, the American Association of Critical-Care Nursesthe American Association of Critical-Care Nurses, the American College of Chest Physiciansthe American College of Chest Physicians, the American College of Emergency Physiciansthe American College of Emergency Physicians, the Canadian Critical Care Societythe Canadian Critical Care Society, the European Society of Clinical Microbiology and Infectious Diseasesthe European Society of Clinical Microbiology and Infectious Diseases, the European Society of Intensive Care Medicinethe European Society of Intensive Care Medicine, the European Respiratory Societythe European Respiratory Society, the International Sepsis Forumthe International Sepsis Forum, the Japanese Association for Acute Medicinethe Japanese Association for Acute Medicine, the Japanese Society of Intensive Care Medicinethe Japanese Society of Intensive Care Medicine, the Society of Critical Care Medicinethe Society of Critical Care Medicine, the Society of Hospital Medicinethe Society of Hospital Medicine, the Surgical Infection Societythe Surgical Infection Society, the World Federation of Societies of Intensive and Critical Care Medicinethe World Federation of Societies of Intensive and Critical Care Medicine.
78. Chung TT, Grossman A, Clark AJL Adrenal insufficiency. Endocrinology Adult and Pediatric 2010, 1853-1863. WB Saunders, St Louis. 6th edn. J.L. Jameson, L.J. De Groot (Eds.).
79. Debaveye Y, Vandenbrande J, Van den Berghe G Endocrine emergencies. The ESC textbook of intensive and acute cardiac care 2011, 709-717. Oxford University Press, New York. M. Tubaro, N. Danchin, G. Filippatos, P. Goldstein, P. Vranckx, D. Zahger (Eds.).
80. Patel GP, Balk RA Systemic steroids in severe sepsis and septic shock. Am J Respir Crit Care Med 2012, 185:133-139.
81. Annane D, Sébille V, Charpentier C, et al. Effect of treatment with low doses of hydrocortisone and fludrocortisone on mortality in patients with septic shock. JAMA 2002, 288:862-871.
82. Sprung CL, Annane D, Keh D, et al. Hydrocortisone therapy for patients with septic shock. N Engl J Med 2008, 358:111-124. the CORTICUS Study Group.
83. Venkatesh B, Myburgh J, Finfer S, et al. The ADRENAL study protocol: adjunctive corticosteroid treatment in critically ill patients with septic shock. Crit Care Resusc 2013, 15:83-88. the ANZICS CTG investigators.