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A 3-Level Prognostic Classification in Septic Shock Based on Cortisol Levels and Cortisol Response to Corticotropin
Abstract
CONTEXT: The hypothalamic-pituitary-adrenal axis is a major determinant of the host response to stress. The relationship between its activation and patient outcome is not known. OBJECTIVE: To evaluate the prognostic value of cortisol levels and a short corticotropin stimulation test in patients with septic shock. DESIGN AND SETTING: Prospective inception cohort study conducted between October 1991 and September 1995 in 2 teaching hospital adult intensive care units in France. PARTICIPANTS: A total of 189 consecutive patients who met clinical criteria for septic shock. INTERVENTION: A short corticotropin stimulation test was performed in all patients by intravenously injecting 0.25 mg of tetracosactrin; blood samples were taken immediately before the test (T0) and 30 (T30) and 60 (T60) minutes afterward. MAIN OUTCOME MEASURES: Twenty-eight-day mortality as a function of variables collected at the onset of septic shock, including cortisol levels before the corticotropin test and the cortisol response to corticotropin (delta max, defined as the difference between T0 and the highest value between T30 and T60). RESULTS: The 28-day mortality was 58% (95% confidence interval [CI], 51%-65%) and median time to death was 17 days (95% CI, 14-27 days). In multivariate analysis, independent predictors of death (P < or = .001 for all) were McCabe score greater than 0, organ system failure score greater than 2, arterial lactate level greater than 2.8 mmol/L, ratio of PaO2 to fraction of inspired oxygen no more than 160 mm Hg, cortisol level at T0 greater than 34 microg/dL and delta max no more than 9 microg/dL. Three groups of patient prognoses were identified: good (cortisol level at T0 < or = 34 microg/dL and delta max > 9 microg/dL; 28-day mortality rate, 26%), intermediate (cortisol level at T0 34 microg/dL and delta max < or = 9 microg/dL or cortisol level at T0 > 34 microg/dL and delta max > 9 microg/dL; 28-day mortality rate, 67%), and poor (cortisol level at T0 > 34 microg/dL and delta max < or = 9 microg/dL; 28-day mortality rate, 82%). CONCLUSION: Our data suggest that a short corticotropin test has a good prognostic value and could be helpful in identifying patients with septic shock at high risk for death.
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“Short-term hormone dysfunction could also be explained by acute phase inflammation and stress49505152.”
From Endocrine dysfunction following traumatic brain injury: a 5-year follow-up nationwide-based study (2016) · cites this paper as [51]
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BackgroundAssessment of adrenal function in cirrhotic patients: Salivary cortisol should be preferred
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“In a prospective inception cohort study of 189 patients who had septic shock, thorough analyses demonstrated that the best definition of occult adrenal insufficiency should be based on a cortisol increment after a short corticotropin test of less than 9 mg/dL (11).”
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“From large association studies, such a condition is thought to be identifiable by an insufficient rise ( 9 g/dL) in plasma cortisol in response to a 250- g ACTH bolus, irrespective of the baseline plasma cortisol concentration, which is usually much higher than in healthy humans (72).”
BackgroundIncreased Risk of Adrenal Insufficiency Following Etomidate Exposure in Critically Injured Patients
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“A recent prospective cohort study in 189 patients with septic shock found that patients with high cortisol levels and a reduced response to adrenocorticotropic hormone (ACTH, corticotropin) have the worst outcome [12] .”
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“1% met the classic criterion that the maximal cortisol concentration must be 20 g/dL to diagnosis AI (5) (D.”
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“Observations supporting a role for endogenous GC in controlling sepsis are that adrenalectomized mice are more susceptible to LPS-induced septic shock [12], and adrenal insufficiency in humans is associated with prolonged sepsis [13,14].”
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“Some studies have suggested that an increment occurs independent of basal cortisol levels [31,82,83], whereas others have suggested that the increment decreases in proportion to baseline [5,84,85].”
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“CIRCI was defined as a cortisol increment to corticotropin of B9 lg/dl (Annane criterion), or was defined as random cortisol \15 lg/dl or a cortisol increment to corticotropin B9 lg/dl, if cortisol at baseline was C15 and B34 lg/dl (Stewart and Cooper criteria).”
BackgroundMethodInfluentialOutcome in elderly patients with severe infection is influenced by sex hormones but not gender
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“A threshold value of cortisol levels to exclude adrenal insufficiency has been suggested to be 34 g/dL (13, 36).”
BackgroundHigh prevalence of decreased cortisol reserve in brain-dead potential organ donors
Dimopoulou, I., Tsagarakis, S., Anthi, A., Milou, E., Ilias, Ι., Stavrakaki, K., Charalambidis, C., Tzanela, M., Orfanos, S. E., Mandragos, K. E., et al. (2003) · Critical Care Medicine · doi:10.1097/01.ccm.0000059644.54819.67 · Cited by 95
“In fact, documented relative adrenal hypofunction has been clearly associated with a higher prevalence of multiple organ failure and increased mortality in critically ill patients (16, 28).”
BackgroundAdjunctive corticosteroid therapy in pediatric severe sepsis: Observations from the RESOLVE study*
Zimmerman, J. J., & Williams, M. D. (2010) · Pediatric Critical Care Medicine · doi:10.1097/pcc.0b013e3181d903f6 · Cited by 96
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Bollaert, P., Fieux, F., Charpentier, C., & L�vy, B. (2003) · Shock · doi:10.1097/00024382-200301000-00003 · Cited by 92
“These two thresholds were considered because previous studies have used either the former (5, 7) or the latter (6, 10).”
BackgroundResultInfluentialManagement of sepsis during the early "golden hours".
Raghavan, M., & Marik, P. (2006) · Journal of Emergency Medicine · doi:10.1016/j.jemermed.2006.05.008 · Cited by 97
The altered adrenal axis and treatment with glucocorticoids during critical illness
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“High cortisol levels reflect severe stress, whereas low levels, at baseline and/or upon ACTH stimulation, could point to an inability to sufficiently respond to stress”
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“Although a handful of studies have demonstrated that lactate measurements are independent predictors of outcome using multivariate analysis of factors, including several clinical severity scores (SOFA score, organ system failure index, and Simplified Acute Physiology Score II) (10, 14, 15, 19, 32), little data exist t…”
MethodACTH and cortisol response to critical illness in term and late preterm newborns
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“Despite multiple attempts to identify these patients using static measures of adrenal function(56-61), none have been shown to be functionally useful at detecting this subset of the population(62).”
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The Neuroendocrine Response to Critical Illness is a Dynamic Process
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“Both very high and low cortisol levels have been associated with increased mortality [72–77].”
BackgroundUpdate on adrenal insufficiency in patients with liver cirrhosis
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“Plasma cortisol is measured in most institutions by immunoassay, and the majority of recent studies in this field have utilised this technique [1, 2, 3, 4].”
MethodEndocrine measurements in survivors and non-survivors from critical illness
Ray, D. C., MacDuff, A., Drummond, G. B., Wilkinson, E., Adams, B., & Beckett, G. J. (2002) · Intensive Care Medicine · doi:10.1007/s00134-002-1427-y · Cited by 82
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Hypothalamic-Pituitary-Adrenal Axis Dysfunction in Hospitalized Neonatal Foals
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Etomidate for emergency anaesthesia; mad, bad and dangerous to know?
Morris, C., & McAllister, C. (2005) · Anaesthesia · doi:10.1111/j.1365-2044.2005.04325.x · Cited by 82
Association between Adrenal Insufficiency and Ventilator Weaning
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du Cheyron, D., Lesage, A., Daubin, C., Ramakers, M., & Charbonneau, P. (2003) · Intensive Care Medicine · doi:10.1007/s00134-003-1986-6 · Cited by 82
“05 (one-tailed hypothesis), assuming that the incidence of hyperreninemic hypoaldosteronism for septic patients may be of the same magnitude as the abnormal cortisol response to corticotropin stimulation (40–50%) [6].”
BackgroundMethodInfluentialEffects of hydrocortisone on microcirculatory alterations in patients with septic shock*
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“Experimental and clinical studies have shown that corticosteroids can restore vascular responsiveness to catecholamines in septic shock (14, 27, 28), leading to a shorter duration of septic shock (11, 13, 19, 29).”
BackgroundDissociation of Serum Dehydroepiandrosterone and Dehydroepiandrosterone Sulfate in Septic Shock
Arlt, W., Hammer, F., Sanning, P., Butcher, S. K., Lord, J. M., Allolio, B., Annane, D., & Stewart, P. M. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2258 · Cited by 82
“gested to be a prognostic marker for higher mortality (3).”
BackgroundSelf-citationRelative Adrenal Insufficiency in Dogs with Sepsis
Burkitt, J. M., Haskins, S. C., Nelson, R. W., & Kass, P. H. (2007) · Journal of Veterinary Internal Medicine · doi:10.1111/j.1939-1676.2007.tb02953.x · Cited by 83
Severe sepsis: Low expression of the renin-angiotensin system is associated with poor prognosis
Zhang, W., Chen, X., Huang, L., Lü, N., Zhou, L., Wu, G.-J., & Chen, Y. (2014) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2014.1566 · Cited by 80
“However, in using this method, patients are more prone to develop organ damage (high SOFA score) or have a high risk of mortality (32).”
Hypopituitarism is uncommon after aneurysmal subarachnoid haemorrhage
Klose, M., Brennum, J., Poulsgaard, L., Kosteljanetz, M., Wagner, A., & Feldt‐Rasmussen, U. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03791.x · Cited by 81
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Self-citationNew insights into the controversy of adrenal function during critical illness
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“In addition, evidence suggests that a longer ( 2 to 3 days) course of low-dose corticosteroid therapy may be of benefit, particularly in septic patients with poor adrenal reserve as measured by the corticotropin stimulation test (12).”
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Corticosteroid after etomidate in critically ill patients
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“The latter could be caused by better characterization of disease severity by ACTH-cortisol responses rather than by the scoring systems used but does not necessarily indicate causality (4, 6, 8, 10, 16, 17).”
BackgroundResultInfluentialHe, X., Ai, S., Guo, W., Yang, Y., Wang, Z., Jiang, D., & Xu, X. M. (2018) · Translational research · doi:10.1016/j.trsl.2018.04.006 · Cited by 73
“The worldwide incidence of sepsis is estimated to be 18 million cases per year, and the death rate of severe sepsis ranges from 30% to 50% despite advances in critical care.(2-6) An effective treatment regimen is desperately needed.”
BackgroundModulation of the renin–angiotensin–aldosterone system in sepsis: a new therapeutic approach?
Salgado, D. R., Rocco, J. R., Silva, E., & Vincent, J. (2009) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903460332 · Cited by 77
“Patients lacking this response are at greater risk of multiple organ failure and death [6,7].”
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Therapeutic approaches to innate immunity: severe sepsis and septic shock
Lolis, E., & Bucala, R. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1153 · Cited by 74
“Interestingly, there is renewed interest in this first-tried therapy, in part because of observations that adrenal function is impaired during sepsi”
BackgroundGuerrero, J., Gatica, H. A., Rodríguez, M., Estay, R., & Goecke, I. A. (2013) · Critical Care · doi:10.1186/cc12774 · Cited by 71
“A renewed interest in GC therapy in sepsis, at what has been termed a physiological dose, was seen after reports of improved response to vasopressor drugs and decreased mortality in selected groups of patients who had an inadequate response to adrenocorticotropin hormone (ACTH) (defined as an increase in total plasma…”
BackgroundTreating Critical Illness: The Importance of First Doing No Harm
Singer, M., & Glynne, P. A. (2005) · PLoS Medicine · doi:10.1371/journal.pmed.0020167 · Cited by 70
Critical issues in endocrinology.
Goldberg, P. A., & Inzucchi, S. (2003) · Clinics in Chest Medicine · doi:10.1016/s0272-5231(03)00091-1 · Cited by 58
A rationale for using steroids in the treatment of severe cases of H5N1 avian influenza
Carter, M. J. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47124-0 · Cited by 71
“If they do not, this would constitute adrenal insufficiency (Annane et al., 2000).”
BackgroundMechanisms and clinical consequences of critical illness associated adrenal insufficiency
Marik, P. E. (2007) · Current Opinion in Critical Care · doi:10.1097/mcc.0b013e32818a6d74 · Cited by 71
Evaluation of plasma catecholamine and serum cortisol concentrations in horses with colic.
Hinchcliff, K., Rush, B., & Farris, J. W. (2005) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.2005.227.276 · Cited by 63
HDL-cholesterol level and cortisol response to synacthen in critically ill patients
van der Voort, P. H. J., Gerritsen, R. T., Bakker, A. J., Boerma, E. C., Kuiper, M. A., & de Heide, L. (2003) · Intensive Care Medicine · doi:10.1007/s00134-003-2021-7 · Cited by 70
Free Cortisol in Sepsis and Septic Shock
Bendel, S., Karlsson, S., Pettilä, V., Loisa, P., Varpula, M., & Ruokonen, E. (2008) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e318172fdba · Cited by 70
“This is in agreement with previous studies.(2,6,15) Moreover, we demonstrated that the calculated free/total cortisol ratio was lower in survivors.”
ResultExperimental and Clinical Studies
Sarkar, N. (2005) · Cited by 70
Measurement of Serum Free Cortisol Shows Discordant Responsivity to Stress and Dynamic Evaluation
Christ‐Crain, M., Jutla, S., Suter‐Widmer, I., Couppis, O., König, C., Pargger, H., Puder, J. J., Edwards, R., Müller-Stich, B. P., & Grossman, A. B. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2361 · Cited by 68
Freitas, I. D., Fernández-Somoza, M., Essenfeld-Sekler, E., & Cardier, J. E. (2004) · CHEST Journal · doi:10.1378/chest.125.6.2238 · Cited by 69
Endocrine and Metabolic Alterations in Sepsis and Implications for Treatment
Ingels, C., Gunst, J., & den Berghe, G. V. (2017) · Critical Care Clinics · doi:10.1016/j.ccc.2017.08.006 · Cited by 69
A Blueprint for a Sepsis Protocol
Shapiro, N. I., Howell, M. D., & Talmor, D. S. (2005) · Academic Emergency Medicine · doi:10.1111/j.1553-2712.2005.tb01957.x · Cited by 68
Metabolic Acidosis in Patients with Sepsis: Epiphenomenon or Part of the Pathophysiology?
Kellum, J. A. (2004) · Critical Care and Resuscitation · doi:10.1016/s1441-2772(23)02175-0 · Cited by 67
Adrenal insufficiency in liver disease - what is the evidence?
O'Beirne, J., Holmes, M., Agarwal, B., Bouloux, P., Shaw, S., Patch, D., & Burroughs, A. (2007) · Journal of Hepatology · doi:10.1016/j.jhep.2007.06.008 · Cited by 65
“Evidence supporting the concept of RAI came from the study by Annane et al. which examined the outcome of 189 septic shock patients who underwent adrenocortical function testing with 250 l go f ACTH[ 8 ].”
BackgroundInfluentialRoy, M. (2004) · Veterinary Clinics of North America Equine Practice · doi:10.1016/j.cveq.2003.12.005 · Cited by 74
Hammond, D. A., Ficek, O. A., Painter, J. T., McCain, K., Cullen, J., Brotherton, A. L., Kakkera, K. S. S., Chopra, D., & Meena, N. K. (2018) · Pharmacotherapy The Journal of Human Pharmacology and Drug Therapy · doi:10.1002/phar.2105 · Cited by 66
Low-dose steroids in adult septic shock: results of the Surviving Sepsis Campaign
Casserly, B. P., Gerlach, H., Phillips, G. S., Lemeshow, S. A., Marshall, J. C., Osborn, T. M., & Levy, M. M. (2012) · Intensive Care Medicine · doi:10.1007/s00134-012-2720-z · Cited by 65
Loisa, P., Uusaro, A. V., & Ruokonen, E. (2005) · Anesthesia & Analgesia · doi:10.1213/01.ane.0000184042.91452.48 · Cited by 65
“Most investigators have introduced their own criteria for the diagnosis of adrenocortical insufficiency (5,7,8), and many of these criteria are broadly similar to the values used in the overall hospital population.”
BackgroundMethodInfluentialThe top cited clinical research articles on sepsis: a bibliometric analysis
Tao, T., Zhao, X., Lou, J., Bo, L., Wang, F., Li, J., & Deng, X. (2012) · Critical Care · doi:10.1186/cc11401 · Cited by 66
den Berghe, G. V., Téblick, A., Langouche, L., & Gunst, J. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104284 · Cited by 74
The Central Role of the Inflammatory Response in Understanding the Heterogeneity of Sepsis-3
Ding, R., Meng, Y., & Ma, X. (2018) · BioMed Research International · doi:10.1155/2018/5086516 · Cited by 68
“It has been established that adrenal insufficiency in sepsis (especially septic shock) is in part responsible for the reduction of vascular reactivity to vasopressors and is associated with an increased risk of death [60].”
BackgroundMagnotti, M., & Shimshi, M. (2008) · Endocrine Practice · doi:10.4158/ep.14.2.233 · Cited by 62
Hypoglycemia and mortality in sepsis patients: A systematic review and meta-analysis
Wang, J., Zhu, C., Yu, J., Tan, R., & Yang, P. (2021) · Heart & Lung · doi:10.1016/j.hrtlng.2021.07.017 · Cited by 63
Jensterle, M., Herman, R., Janež, A., Mahmeed, W. A., Al‐Rasadi, K., Al-Alawi, K., Banach, M., Banerjee, Y., Ceriello, A., Cesur, M., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137326 · Cited by 64
“in septic shock [31], later named critical illness-related corticosteroid insufficiency (CIRCI) [32].”
BackgroundLow-dose hydrocortisone in pediatric septic shock: An exploratory study in a third world setting
Valoor, H. T., Singhi, S. C., & Jayashree, M. (2009) · Pediatric Critical Care Medicine · doi:10.1097/pcc.0b013e3181936ab3 · Cited by 61
“The primary concern that emerge from all this is whether patients with intact HPA axis should receive corticosteroids since several studies have shown that nearly half of patients in septic shock are corticotropin responders (29, 30).”
BackgroundAdrenal insufficiency in the critically ill neonate and child
Langer, M., Modi, B. P., & Agus, M. S. D. (2006) · Current Opinion in Pediatrics · doi:10.1097/01.mop.0000236397.79580.85 · Cited by 61
Zhang, Q., Dong, G., Zhao, X., Wang, M., & Li, C.-S. (2014) · Intensive Care Medicine · doi:10.1007/s00134-014-3468-4 · Cited by 62
“62 with a cutoff value of 34 lg/dl [5, 7].”
BackgroundResultEndocrine predictors of mortality in canine babesiosis caused by Babesia canis rossi
Schoeman, J. P., Rees, P., & HERRTAGE, M. E. (2007) · Veterinary Parasitology · doi:10.1016/j.vetpar.2007.06.010 · Cited by 61
Venkatesh, B., Myburgh, J., Finfer, S. R., Webb, S. A. R., Cohen, J., Bellomo, R., McArthur, C. J., Joyce, C., Rajbhandari, D., Glass, P., et al. (2013) · Critical Care and Resuscitation · doi:10.1016/s1441-2772(23)01786-6 · Cited by 60
Critical Illness–induced Corticosteroid Insufficiency: What It Is Not and What It Could Be
Téblick, A., Gunst, J., & den Berghe, G. V. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac201 · Cited by 64
Cohen, J., Pretorius, C. J., Ungerer, J. P. J., Cardinal, J., Blumenthal, A., Presneill, J., Gatica-Andrades, M., Jarrett, P., Lassig-Smith, M., Stuart, J., et al. (2016) · Critical Care Medicine · doi:10.1097/ccm.0000000000001633 · Cited by 58
“Previous work has indicated that higher total plasma cortisol levels are associated with worse outcomes (11).”
BackgroundMorel, J., Salard, M., Castelain, C., Bayon, M. C., Lambert, P., Vola, M., Auboyer, C., & Molliex, S. B. (2011) · British Journal of Anaesthesia · doi:10.1093/bja/aer169 · Cited by 59
Metadata
- Authors
- Annane, D.
- Affiliations
- Hôpital Raymond-Poincaré (FR)
- Corresponding author
- Annane, Djillali
- ORCID
- Annane, Djillali
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2000-02-23
- Volume
- 283
- Issue
- 8
- Pages
- 1038
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- OpenAlex
- W2156618518
- Cited by
- 1,000
- References
- 40
- Citations by year
- 2026: 11 · 2025: 17 · 2024: 15 · 2023: 19 · 2022: 15 · 2021: 13 · 2020: 19 · 2019: 22 · 2018: 27 · 2017: 27 · 2016: 27 · 2015: 26 · 2014: 44 · 2013: 35 · 2012: 38
- FWCI
- 38.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Sepsis Diagnosis and Treatment
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hyperglycemia and glycemic control in critically ill and hospitalized patients
- Keywords
- septic shock, cortisol, ACTH stimulation test, tetracosactrin, hypothalamic-pituitary-adrenal axis, prognostic stratification, 28-day mortality, stress response, organ failure, lactate, PaO2/FiO2 ratio, intensive care unit patients, corticosteroid therapy, sepsis
- MeSH terms
- Adult, Cosyntropin, Female, Humans, Hydrocortisone, Hypothalamo-Hypophyseal System, Male, Middle Aged, Pituitary-Adrenal System, Prognosis, Prospective Studies, Severity of Illness Index, Shock, Septic, Biomarkers, Multivariate Analysis, Proportional Hazards Models, Survival Analysis
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