{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,14]],"date-time":"2026-05-14T04:11:50Z","timestamp":1778731910532,"version":"3.51.4"},"reference-count":36,"publisher":"MDPI AG","issue":"20","license":[{"start":{"date-parts":[[2024,10,11]],"date-time":"2024-10-11T00:00:00Z","timestamp":1728604800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"departmental resources"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Background: Energy expenditure (EE) in patients with aneurysmal subarachnoid hemorrhage (SAH) may differ from other intracranial pathologies, such as intracerebral hemorrhage (ICH) or traumatic brain injury (TBI), due to an activation of the sympathetic nervous system. Indirect calorimetry (IC) is recommended, but is not always available. We study EE, catabolism, and metabolic stress in patients with SAH, TBI, ICH, and sepsis as controls. Methods: A prospective observational study was conducted in the intensive care units of the University Medical Center Hamburg-Eppendorf, Germany. IC was used to measure EE on days 2\u20133, 5\u20137, and 10\u201315 post-admission. Urinary catecholamines, metabolites, and urine urea were also measured. Statistical analysis included t-tests, Chi-square tests, and generalized mixed models. Results: We included 110 patients\u201443 SAH patients (13 with the surgical securing of the aneurysm and 30 with coil embolization of the aneurysm), 22 TBI patients, 23 ICH patients, and 22 controls. The generalized linear mixed model analysis for groups and timepoints including age, height, and weight as covariates revealed a significantly lower EE at timepoint 1 for ICH versus SAH\u2014interventional (p = 0.003) and versus the control (p = 0.004), as well as at timepoint 2 for ICH versus SAH\u2014interventional (p = 0.002) and versus SAH\u2014surgical (p = 0.013) with a lower EE in ICH patients. No significant differences between groups were found for EE at the other timepoints, or concerning urine urea and measurements of catecholamines in urine. Conclusions: In patients with SAH, ICH, and TBI, no meaningful differences in EE were detected compared to septic critically ill patients, except for a lower EE in ICH patients in the early phase.<\/jats:p>","DOI":"10.3390\/nu16203448","type":"journal-article","created":{"date-parts":[[2024,10,11]],"date-time":"2024-10-11T08:10:16Z","timestamp":1728634216000},"page":"3448","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Energy Expenditure in Critically Ill Patients with Aneurysmal Subarachnoid Hemorrhage, Intracerebral Hemorrhage, and Traumatic Brain Injury\u2014A Prospective Observational Study"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1950-8683","authenticated-orcid":false,"given":"Geraldine","family":"de Heer","sequence":"first","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna Leonie","family":"Doliwa","sequence":"additional","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pascal","family":"Hilbert","sequence":"additional","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7530-8155","authenticated-orcid":false,"given":"Marlene","family":"Fischer","sequence":"additional","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0865-241X","authenticated-orcid":false,"given":"Patrick","family":"Czorlich","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nils","family":"Schweingruber","sequence":"additional","affiliation":[{"name":"Department of Neurology, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stefan","family":"Kluge","sequence":"additional","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christoph","family":"Burdelski","sequence":"additional","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3341-669X","authenticated-orcid":false,"given":"J\u00f6rn","family":"Grensemann","sequence":"additional","affiliation":[{"name":"Department of Intensive Care Medicine, University Medical Center Hamburg-Eppendorf, Martinistra\u00dfe 52, 20246 Hamburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1177\/0148607114567898","article-title":"Prevalence of Underprescription or Overprescription of Energy Needs in Critically Ill Mechanically Ventilated Adults as Determined by Indirect Calorimetry: A Systematic Literature Review","volume":"40","author":"Ridley","year":"2016","journal-title":"JPEN J. Parenter. Enter. Nutr."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.clnu.2018.08.037","article-title":"ESPEN guideline on clinical nutrition in the intensive care unit","volume":"38","author":"Singer","year":"2019","journal-title":"Clin. Nutr."},{"key":"ref_3","unstructured":"AWMF (2019, June 24). S2k-Leitlinie: Klinische Ern\u00e4hrung in der Intensivmedizin, Registernummer 073-004. Available online: https:\/\/register.awmf.org\/assets\/guidelines\/073-004m_S2k_Klinische-Ernaehrung-Intensivmedizin_2018-11-1-abgelaufen.pdf."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1206","DOI":"10.1016\/j.clnu.2018.04.020","article-title":"Predictive equations versus measured energy expenditure by indirect calorimetry: A retrospective validation","volume":"38","author":"Zusman","year":"2019","journal-title":"Clin. Nutr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1178638820903295","DOI":"10.1177\/1178638820903295","article-title":"Is Energy Delivery Guided by Indirect Calorimetry Associated with Improved Clinical Outcomes in Critically Ill Patients? A Systematic Review and Meta-analysis","volume":"13","author":"Fetterplace","year":"2020","journal-title":"Nutr. Metab. Insights"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1955","DOI":"10.1007\/s00134-006-0408-y","article-title":"Sympathetic activation and inflammatory response in patients with subarachnoid haemorrhage","volume":"32","author":"Naredi","year":"2006","journal-title":"Intensive Care Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"710","DOI":"10.3171\/jns.1990.72.5.0710","article-title":"Hypermetabolism in the acute stage of hemorrhagic cerebrovascular disease","volume":"72","author":"Touho","year":"1990","journal-title":"J. Neurosurg."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1186\/s13613-024-01350-x","article-title":"Nutritional and metabolic modulation of inflammation in critically ill patients: A narrative review of rationale, evidence and grey areas","volume":"14","author":"Rousseau","year":"2024","journal-title":"Ann. Intensive Care"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Morbitzer, K.A., Wilson, W.S., Chaben, A.C., Darby, A., Dehne, K.A., Brown, E.R., Rhoney, D.H., and Jordan, J.D. (2019). Energy Expenditure in Critically Ill Adult Patients with Acute Brain Injury: Indirect Calorimetry vs. Predictive Equations. Front. Neurol., 10.","DOI":"10.3389\/fneur.2019.01426"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1212\/WNL.0000000000001259","article-title":"Inflammation, negative nitrogen balance, and outcome after aneurysmal subarachnoid hemorrhage","volume":"84","author":"Badjatia","year":"2015","journal-title":"Neurology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1080\/03009734.2019.1659888","article-title":"Daily systemic energy expenditure in the acute phase of aneurysmal subarachnoid hemorrhage","volume":"124","author":"Nyberg","year":"2019","journal-title":"Upsala J. Med. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s00701-017-3400-0","article-title":"Systemic metabolism and energy consumption after microsurgical clipping and endovascular coiling for aneurysmal subarachnoid hemorrhage","volume":"160","author":"Tosaka","year":"2018","journal-title":"Acta Neurochir."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1111\/ene.13265","article-title":"Impact of dexamethasone in patients with aneurysmal subarachnoid haemorrhage","volume":"24","author":"Czorlich","year":"2017","journal-title":"Eur. J. Neurol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1001\/jama.2016.0287","article-title":"The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3)","volume":"315","author":"Singer","year":"2016","journal-title":"JAMA"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.3945\/ajcn.111.023390","article-title":"How much protein do parenteral amino acid mixtures provide?","volume":"94","author":"Hoffer","year":"2011","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1055\/a-1030-5207","article-title":"Leitfaden Ern\u00e4hrungstherapie in Klinik und Praxis (LEKuP)","volume":"44","author":"Hauner","year":"2019","journal-title":"Aktuelle Ern\u00e4hrungsmed."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/j.nut.2004.07.005","article-title":"Predicting total urinary nitrogen excretion from urinary urea nitrogen excretion in multiple-trauma patients receiving specialized nutritional support","volume":"21","author":"Dickerson","year":"2005","journal-title":"Nutrition"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1186\/s13054-016-1538-4","article-title":"Resting energy expenditure, calorie and protein consumption in critically ill patients: A retrospective cohort study","volume":"20","author":"Zusman","year":"2016","journal-title":"Crit. Care"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1177\/0885066620966957","article-title":"Relationship between Nutrition Intake and Outcome after Subarachnoid Hemorrhage: Results from the International Nutritional Survey","volume":"36","author":"Badjatia","year":"2021","journal-title":"J. Intensive Care Med."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Shestopalov, A.E., Yakovleva, A.V., Yadgarov, M.Y., Sergeev, I.V., and Kuzovlev, A.N. (2024). Prevalence and Impact of Malnutrition Risk on Outcomes in Critically Ill Patients with Traumatic Brain Injury and Stroke: A Retrospective Cohort Study Using Electronic Health Records. Nutrients, 16.","DOI":"10.3390\/nu16152396"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1186\/s13054-021-03508-6","article-title":"Energy delivery guided by indirect calorimetry in critically ill patients: A systematic review and meta-analysis","volume":"25","author":"Duan","year":"2021","journal-title":"Crit. Care"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00063-023-01001-2","article-title":"Laborchemisches und kalorimetrisches Monitoring der medizinischen Ern\u00e4hrungstherapie auf der Intensiv- und Intermediate Care Station","volume":"118","author":"Elke","year":"2023","journal-title":"Med. Klin. Intensivmed. Notfallmed."},{"key":"ref_23","first-page":"30","article-title":"Clinical Guide for the Use of Metabolic Carts: Indirect Calorimetry\u2014No Longer the Orphan of Energy Estimation","volume":"31","author":"Singer","year":"2016","journal-title":"Nutr. Clin. Pract. Off. Publ. Am. Soc. Parenter. Enter. Nutr."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1007\/s12028-012-9673-5","article-title":"Determinants of central sympathetic activation in spontaneous primary subarachnoid hemorrhage","volume":"16","author":"Moussouttas","year":"2012","journal-title":"Neurocrit. Care"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1016\/j.jstrokecerebrovasdis.2015.12.008","article-title":"Increased Resting Energy Expenditure after Endovascular Coiling for Subarachnoid Hemorrhage","volume":"25","author":"Nagano","year":"2016","journal-title":"J. Stroke Cerebrovasc. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1097\/00003246-199310000-00018","article-title":"Effects of norepinephrine, epinephrine, and dopamine infusions on oxygen consumption in volunteers","volume":"21","author":"Ensinger","year":"1993","journal-title":"Crit. Care Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1007\/BF02425154","article-title":"Are the effects of noradrenaline, adrenaline and dopamine infusions on VO2 and metabolism transient?","volume":"21","author":"Ensinger","year":"1995","journal-title":"Intensive Care Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2147","DOI":"10.1001\/jama.2022.20521","article-title":"Progress and Challenges in Bacterial Meningitis: A Review","volume":"328","author":"Hasbun","year":"2022","journal-title":"JAMA"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2955","DOI":"10.1007\/s10787-023-01361-3","article-title":"A narrative review of the effects of dexamethasone on traumatic brain injury in clinical and animal studies: Focusing on inflammation","volume":"31","author":"Soltani","year":"2023","journal-title":"Inflammopharmacology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"81","DOI":"10.3171\/jns.1986.64.1.0081","article-title":"Effect of high-dose dexamethasone on outcome from severe head injury","volume":"64","author":"Dearden","year":"1986","journal-title":"J. Neurosurg."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1177\/17474930221093501","article-title":"Fight INflammation to Improve outcome after aneurysmal Subarachnoid HEmorRhage (FINISHER) trial: Study protocol for a randomized controlled trial","volume":"18","author":"Lampmann","year":"2023","journal-title":"Int. J. Stroke"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1097\/00006123-199806000-00038","article-title":"Metabolic profiles of patients with subarachnoid hemorrhage treated by early surgery","volume":"42","author":"Kasuya","year":"1998","journal-title":"Neurosurgery"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e421","DOI":"10.1212\/WNL.0000000000005902","article-title":"Serum glutamine and hospital-acquired infections after aneurysmal subarachnoid hemorrhage","volume":"91","author":"Badjatia","year":"2018","journal-title":"Neurology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"136","DOI":"10.4037\/ajcc2019168","article-title":"Resting Energy Expenditure and Oxygen Consumption in Critically Ill Patients with vs without Sepsis","volume":"28","author":"Menegueti","year":"2019","journal-title":"Am. J. Crit. Care"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1186\/s13054-020-03245-2","article-title":"Substrate utilization and energy expenditure pattern in sepsis by indirect calorimetry","volume":"24","author":"Li","year":"2020","journal-title":"Crit. Care"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"45s","DOI":"10.1016\/S0899-9007(97)00205-0","article-title":"Energy metabolism in sepsis and injury","volume":"13","author":"Revelly","year":"1997","journal-title":"Nutrition"}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/16\/20\/3448\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:11:18Z","timestamp":1760112678000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/16\/20\/3448"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,11]]},"references-count":36,"journal-issue":{"issue":"20","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["nu16203448"],"URL":"https:\/\/doi.org\/10.3390\/nu16203448","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,11]]}}}