Skip to main content
Top
Published in: BMC Anesthesiology 1/2023

Open Access 01-12-2023 | Septicemia | Research

Long-term clinical outcomes in critically ill patients with sepsis and pre-existing low muscle mass: a retrospective cohort study

Authors: Nola Darden, Sonakshi Sharma, Xue Wu, Benjamin Mancini, Kunal Karamchandani, Anthony S. Bonavia

Published in: BMC Anesthesiology | Issue 1/2023

Login to get access

Abstract

Purpose

Critically ill patients with sepsis account for significant disease morbidity and healthcare costs. Low muscle mass has been proposed as an independent risk factor for poor short-term outcomes, although its effect on long-term outcomes remains unclear.

Methods

Retrospective cohort analysis of patients treated at a quaternary care medical center over 6 years (09/2014 - 12/2020). Critically ill patients meeting Sepsis-3 criteria were included, with low muscle mass defined by \(\le\) 5th percentile skeletal muscle index, measured at the L3 lumbar level (L3SMI) on Computed-Tomography (CT) scan (\(\le\) 41.6 cm2/m2 for males and \(\le\) 32.0 cm2/m2 for females). L3SMI was calculated by normalizing the CT-measured skeletal muscle area to the square of the patient’s height (in meters). Measurements were taken from abdominal/pelvic CT scan obtained within 7 days of sepsis onset. The prevalence of low muscle mass and its association with clinical outcomes, including in-hospital and one-year mortality, and post-hospitalization discharge disposition in survivors, was analyzed. Unfavorable post-hospitalization disposition was defined as discharge to a location other than the patient’s home.

Results

Low muscle mass was present in 34 (23%) of 150 patients, with mean skeletal muscle indices of 28.0 ± 2.9 cm2/m2 and 36.8 ± 3.3 cm2/m2 in females and males, respectively. While low muscle mass was not a significant risk factor for in-hospital mortality (hazard ratio 1.33; 95% CI 0.64 – 2.76; p = 0.437), it significantly increased one-year mortality after adjusting for age and illness severity using Cox multivariate regression (hazard ratio 1.9; 95% CI 1.1 – 3.2; p = 0.014). Unfavorable post-hospitalization discharge disposition was not associated with low muscle mass, after adjusting for age and illness severity in a single, multivariate model.

Conclusion

Low muscle mass independently predicts one-year mortality but is not associated with in-hospital mortality or unfavorable hospital discharge disposition in critically ill patients with sepsis.
Literature
1.
go back to reference Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):801–10.CrossRefPubMedPubMedCentral Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):801–10.CrossRefPubMedPubMedCentral
2.
go back to reference Lu J, Liu J, Zhu L, Zhang Y, Li A. The effect of age on the clinical characteristics and innate immune cell function in the patients with abdominal sepsis. Front Physiol. 2022;13:952434.PubMedPubMedCentral Lu J, Liu J, Zhu L, Zhang Y, Li A. The effect of age on the clinical characteristics and innate immune cell function in the patients with abdominal sepsis. Front Physiol. 2022;13:952434.PubMedPubMedCentral
3.
go back to reference Rantanen T. Muscle strength, disability and mortality. Scand J Med Sci Sports. 2003;13(1):3–8.PubMed Rantanen T. Muscle strength, disability and mortality. Scand J Med Sci Sports. 2003;13(1):3–8.PubMed
4.
go back to reference Sakuma K, Aoi W, Yamaguchi A. Current understanding of sarcopenia: possible candidates modulating muscle mass. Pflugers Arch. 2015;467(2):213–29.PubMed Sakuma K, Aoi W, Yamaguchi A. Current understanding of sarcopenia: possible candidates modulating muscle mass. Pflugers Arch. 2015;467(2):213–29.PubMed
5.
go back to reference Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol. 2012;3:260.PubMedPubMedCentral Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol. 2012;3:260.PubMedPubMedCentral
6.
go back to reference Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412–23.PubMedPubMedCentral Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412–23.PubMedPubMedCentral
7.
go back to reference Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(4):601.PubMedPubMedCentral Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(4):601.PubMedPubMedCentral
8.
go back to reference Portal D, Hofstetter L, Eshed I, Dan-Lantsman C, Sella T, Urban D, et al. L3 skeletal muscle index (L3SMI) is a surrogate marker of sarcopenia and frailty in non-small cell lung cancer patients. Cancer Manag Res. 2019;11:2579–88.PubMedPubMedCentral Portal D, Hofstetter L, Eshed I, Dan-Lantsman C, Sella T, Urban D, et al. L3 skeletal muscle index (L3SMI) is a surrogate marker of sarcopenia and frailty in non-small cell lung cancer patients. Cancer Manag Res. 2019;11:2579–88.PubMedPubMedCentral
9.
go back to reference Portal D, Melamed G, Segal G, Itelman E. Sarcopenia as Manifested by L3SMI Is Associated with Increased Long-Term Mortality amongst Internal Medicine Patients-A Prospective Cohort Study. J Clin Med. 2022;11(12):3500.PubMedPubMedCentral Portal D, Melamed G, Segal G, Itelman E. Sarcopenia as Manifested by L3SMI Is Associated with Increased Long-Term Mortality amongst Internal Medicine Patients-A Prospective Cohort Study. J Clin Med. 2022;11(12):3500.PubMedPubMedCentral
10.
go back to reference Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, et al. Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (1985). 2004;97(6):2333–8.PubMed Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, et al. Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (1985). 2004;97(6):2333–8.PubMed
11.
go back to reference Scafoglieri A, Clarys JP. Dual energy X-ray absorptiometry: gold standard for muscle mass? J Cachexia Sarcopenia Muscle. 2018;9(4):786–7.PubMedPubMedCentral Scafoglieri A, Clarys JP. Dual energy X-ray absorptiometry: gold standard for muscle mass? J Cachexia Sarcopenia Muscle. 2018;9(4):786–7.PubMedPubMedCentral
12.
go back to reference Stokes T, Tripp TR, Murphy K, Morton RW, Oikawa SY, Lam Choi H, et al. Methodological considerations for and validation of the ultrasonographic determination of human skeletal muscle hypertrophy and atrophy. Physiol Rep. 2021;9(1):e14683.PubMedPubMedCentral Stokes T, Tripp TR, Murphy K, Morton RW, Oikawa SY, Lam Choi H, et al. Methodological considerations for and validation of the ultrasonographic determination of human skeletal muscle hypertrophy and atrophy. Physiol Rep. 2021;9(1):e14683.PubMedPubMedCentral
13.
go back to reference Joskova V, Patkova A, Havel E, Najpaverova S, Uramova D, Kovarik M, et al. Critical Evaluation of Muscle Mass Loss as a Prognostic Marker of Morbidity in Critically Ill Patients and Methods for Its Determination. J Rehabil Med. 2018;50(8):696–704.PubMed Joskova V, Patkova A, Havel E, Najpaverova S, Uramova D, Kovarik M, et al. Critical Evaluation of Muscle Mass Loss as a Prognostic Marker of Morbidity in Critically Ill Patients and Methods for Its Determination. J Rehabil Med. 2018;50(8):696–704.PubMed
14.
go back to reference Sergi G, De Rui M, Stubbs B, Veronese N, Manzato E. Measurement of lean body mass using bioelectrical impedance analysis: a consideration of the pros and cons. Aging Clin Exp Res. 2017;29(4):591–7.PubMed Sergi G, De Rui M, Stubbs B, Veronese N, Manzato E. Measurement of lean body mass using bioelectrical impedance analysis: a consideration of the pros and cons. Aging Clin Exp Res. 2017;29(4):591–7.PubMed
15.
go back to reference Shibahashi K, Sugiyama K, Kashiura M, Hamabe Y. Decreasing skeletal muscle as a risk factor for mortality in elderly patients with sepsis: a retrospective cohort study. J Intensive Care. 2017;5:8.PubMedPubMedCentral Shibahashi K, Sugiyama K, Kashiura M, Hamabe Y. Decreasing skeletal muscle as a risk factor for mortality in elderly patients with sepsis: a retrospective cohort study. J Intensive Care. 2017;5:8.PubMedPubMedCentral
16.
go back to reference Baggerman MR, van Dijk DPJ, Winkens B, van Gassel RJJ, Bol ME, Schnabel RM, et al. Muscle wasting associated co-morbidities, rather than sarcopenia are risk factors for hospital mortality in critical illness. J Crit Care. 2020;56:31–6.PubMed Baggerman MR, van Dijk DPJ, Winkens B, van Gassel RJJ, Bol ME, Schnabel RM, et al. Muscle wasting associated co-morbidities, rather than sarcopenia are risk factors for hospital mortality in critical illness. J Crit Care. 2020;56:31–6.PubMed
17.
go back to reference Liu W, Hu CH, Zhao SP. Sarcopenia and mortality risk of patients with sepsis: a meta-analysis. Int J Clin Pract. 2022;2022:4974410.PubMedPubMedCentral Liu W, Hu CH, Zhao SP. Sarcopenia and mortality risk of patients with sepsis: a meta-analysis. Int J Clin Pract. 2022;2022:4974410.PubMedPubMedCentral
18.
go back to reference Kahn JM, Le T, Angus DC, Cox CE, Hough CL, White DB, et al. The epidemiology of chronic critical illness in the United States*. Crit Care Med. 2015;43(2):282–7.PubMedPubMedCentral Kahn JM, Le T, Angus DC, Cox CE, Hough CL, White DB, et al. The epidemiology of chronic critical illness in the United States*. Crit Care Med. 2015;43(2):282–7.PubMedPubMedCentral
19.
go back to reference Kline KA, Bowdish DM. Infection in an aging population. Curr Opin Microbiol. 2016;29:63–7.PubMed Kline KA, Bowdish DM. Infection in an aging population. Curr Opin Microbiol. 2016;29:63–7.PubMed
20.
go back to reference Jolley RJ, Sawka KJ, Yergens DW, Quan H, Jette N, Doig CJ. Validity of administrative data in recording sepsis: a systematic review. Crit Care. 2015;19(1):139.PubMedPubMedCentral Jolley RJ, Sawka KJ, Yergens DW, Quan H, Jette N, Doig CJ. Validity of administrative data in recording sepsis: a systematic review. Crit Care. 2015;19(1):139.PubMedPubMedCentral
21.
go back to reference Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348(16):1546–54.PubMed Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348(16):1546–54.PubMed
22.
go back to reference Ferreira FL, Bota DP, Bross A, Melot C, Vincent JL. Serial evaluation of the SOFA score to predict outcome in critically ill patients. Jama-J Am Med Assoc. 2001;286(14):1754–8. Ferreira FL, Bota DP, Bross A, Melot C, Vincent JL. Serial evaluation of the SOFA score to predict outcome in critically ill patients. Jama-J Am Med Assoc. 2001;286(14):1754–8.
23.
go back to reference Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13(10):818–29.PubMed Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13(10):818–29.PubMed
24.
go back to reference von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4(10):e296. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4(10):e296.
25.
go back to reference van der Werf A, Langius JAE, de van der Schueren MAE, Nurmohamed SA, van der Pant K, Blauwhoff-Buskermolen S, et al. Percentiles for skeletal muscle index, area and radiation attenuation based on computed tomography imaging in a healthy Caucasian population. Eur J Clin Nutr. 2018;72(2):288–96.PubMed van der Werf A, Langius JAE, de van der Schueren MAE, Nurmohamed SA, van der Pant K, Blauwhoff-Buskermolen S, et al. Percentiles for skeletal muscle index, area and radiation attenuation based on computed tomography imaging in a healthy Caucasian population. Eur J Clin Nutr. 2018;72(2):288–96.PubMed
26.
go back to reference Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.PubMedPubMedCentral Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.PubMedPubMedCentral
27.
go back to reference Gomez-Perez S, McKeever L, Sheean P. Tutorial: a step-by-step guide (version 2.0) for measuring abdominal circumference and skeletal muscle from a single cross-sectional computed-tomography image using the National Institutes of Health ImageJ. J Parenter Enteral Nutr. 2020;44(3):419–24. Gomez-Perez S, McKeever L, Sheean P. Tutorial: a step-by-step guide (version 2.0) for measuring abdominal circumference and skeletal muscle from a single cross-sectional computed-tomography image using the National Institutes of Health ImageJ. J Parenter Enteral Nutr. 2020;44(3):419–24.
28.
go back to reference Gomez-Perez SL, Haus JM, Sheean P. Measuring abdominal circumference and skeletal muscle from a single cross-sectional computed tomography image: a step-by-step guide for clinicians using National Institutes of Health ImageJ (vol 40, pg 308, 2016). J Parenter Enteral Nutr. 2016;40(5):742–3. Gomez-Perez SL, Haus JM, Sheean P. Measuring abdominal circumference and skeletal muscle from a single cross-sectional computed tomography image: a step-by-step guide for clinicians using National Institutes of Health ImageJ (vol 40, pg 308, 2016). J Parenter Enteral Nutr. 2016;40(5):742–3.
29.
go back to reference Prest J, Sathananthan M, Jeganathan N. Current trends in sepsis-related mortality in the United States. Crit Care Med. 2021;49(8):1276–84.PubMed Prest J, Sathananthan M, Jeganathan N. Current trends in sepsis-related mortality in the United States. Crit Care Med. 2021;49(8):1276–84.PubMed
30.
go back to reference Kotfis K, Wittebole X, Jaschinski U, Sole-Violan J, Kashyap R, Leone M, et al. A worldwide perspective of sepsis epidemiology and survival according to age: Observational data from the ICON audit. J Crit Care. 2019;51:122–32.PubMed Kotfis K, Wittebole X, Jaschinski U, Sole-Violan J, Kashyap R, Leone M, et al. A worldwide perspective of sepsis epidemiology and survival according to age: Observational data from the ICON audit. J Crit Care. 2019;51:122–32.PubMed
31.
go back to reference Alvarez-Bustos A, Rodriguez-Sanchez B, Carnicero-Carreno JA, Sepulveda-Loyola W, Garcia-Garcia FJ, Rodriguez-Manas L. Healthcare cost expenditures associated to frailty and sarcopenia. BMC Geriatr. 2022;22(1):747.PubMedPubMedCentral Alvarez-Bustos A, Rodriguez-Sanchez B, Carnicero-Carreno JA, Sepulveda-Loyola W, Garcia-Garcia FJ, Rodriguez-Manas L. Healthcare cost expenditures associated to frailty and sarcopenia. BMC Geriatr. 2022;22(1):747.PubMedPubMedCentral
32.
go back to reference Tjeertes EKM, van Fessem JMK, Mattace-Raso FUS, Hoofwijk AGM, Stolker RJ, Hoeks SE. Influence of frailty on outcome in older patients undergoing non-cardiac surgery - a systematic review and meta-analysis. Aging Dis. 2020;11(5):1276–90.PubMedPubMedCentral Tjeertes EKM, van Fessem JMK, Mattace-Raso FUS, Hoofwijk AGM, Stolker RJ, Hoeks SE. Influence of frailty on outcome in older patients undergoing non-cardiac surgery - a systematic review and meta-analysis. Aging Dis. 2020;11(5):1276–90.PubMedPubMedCentral
33.
go back to reference Oh HJ, Kim JH, Kim HR, Ahn JY, Jeong SJ, Ku NS, et al. The impact of sarcopenia on short-term and long-term mortality in patients with septic shock. J Cachexia Sarcopenia Muscle. 2022;13(4):2054–63.PubMedPubMedCentral Oh HJ, Kim JH, Kim HR, Ahn JY, Jeong SJ, Ku NS, et al. The impact of sarcopenia on short-term and long-term mortality in patients with septic shock. J Cachexia Sarcopenia Muscle. 2022;13(4):2054–63.PubMedPubMedCentral
34.
go back to reference Shankar-Hari M, Phillips GS, Levy ML, Seymour CW, Liu VX, Deutschman CS, et al. Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8):775–87.PubMedPubMedCentral Shankar-Hari M, Phillips GS, Levy ML, Seymour CW, Liu VX, Deutschman CS, et al. Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8):775–87.PubMedPubMedCentral
35.
go back to reference Cox MC, Booth M, Ghita G, Wang Z, Gardner A, Hawkins RB, et al. The impact of sarcopenia and acute muscle mass loss on long-term outcomes in critically ill patients with intra-abdominal sepsis. J Cachexia Sarcopenia Muscle. 2021;12(5):1203–13.PubMedPubMedCentral Cox MC, Booth M, Ghita G, Wang Z, Gardner A, Hawkins RB, et al. The impact of sarcopenia and acute muscle mass loss on long-term outcomes in critically ill patients with intra-abdominal sepsis. J Cachexia Sarcopenia Muscle. 2021;12(5):1203–13.PubMedPubMedCentral
36.
go back to reference Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, et al. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310(15):1591–600.PubMed Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, et al. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310(15):1591–600.PubMed
37.
go back to reference Prado CM, Purcell SA, Alish C, Pereira SL, Deutz NE, Heyland DK, et al. Implications of low muscle mass across the continuum of care: a narrative review. Ann Med. 2018;50(8):675–93.PubMed Prado CM, Purcell SA, Alish C, Pereira SL, Deutz NE, Heyland DK, et al. Implications of low muscle mass across the continuum of care: a narrative review. Ann Med. 2018;50(8):675–93.PubMed
38.
go back to reference Moisey LL, Mourtzakis M, Cotton BA, Premji T, Heyland DK, Wade CE, et al. Skeletal muscle predicts ventilator-free days, ICU-free days, and mortality in elderly ICU patients. Crit Care. 2013;17(5):R206.PubMedPubMedCentral Moisey LL, Mourtzakis M, Cotton BA, Premji T, Heyland DK, Wade CE, et al. Skeletal muscle predicts ventilator-free days, ICU-free days, and mortality in elderly ICU patients. Crit Care. 2013;17(5):R206.PubMedPubMedCentral
39.
go back to reference Weijs PJM, Looijaard WGPM, Dekker IM, Stapel SN, Girbes AR, Oudemans-van Straaten HM, et al. Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients. Crit Care. 2014;18(2):R12. Weijs PJM, Looijaard WGPM, Dekker IM, Stapel SN, Girbes AR, Oudemans-van Straaten HM, et al. Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients. Crit Care. 2014;18(2):R12.
40.
go back to reference Akahoshi T, Yasuda M, Momii K, Kubota K, Shono Y, Kaku N, et al. Sarcopenia is a predictive factor for prolonged intensive care unit stays in high-energy blunt trauma patients. Acute Med Surg. 2016;3(4):326–31.PubMedPubMedCentral Akahoshi T, Yasuda M, Momii K, Kubota K, Shono Y, Kaku N, et al. Sarcopenia is a predictive factor for prolonged intensive care unit stays in high-energy blunt trauma patients. Acute Med Surg. 2016;3(4):326–31.PubMedPubMedCentral
41.
go back to reference Chiolero R, Revelly JP, Tappy L. Energy metabolism in sepsis and injury. Nutrition. 1997;13(9 Suppl):45S-51S.PubMed Chiolero R, Revelly JP, Tappy L. Energy metabolism in sepsis and injury. Nutrition. 1997;13(9 Suppl):45S-51S.PubMed
42.
go back to reference Hasselgren PO, Menconi MJ, Fareed MU, Yang H, Wei W, Evenson A. Novel aspects on the regulation of muscle wasting in sepsis. Int J Biochem Cell Biol. 2005;37(10):2156–68.PubMed Hasselgren PO, Menconi MJ, Fareed MU, Yang H, Wei W, Evenson A. Novel aspects on the regulation of muscle wasting in sepsis. Int J Biochem Cell Biol. 2005;37(10):2156–68.PubMed
43.
go back to reference Gomes F, Baumgartner A, Bounoure L, Bally M, Deutz NE, Greenwald JL, et al. Association of nutritional support with clinical outcomes among medical inpatients who are malnourished or at nutritional risk an updated systematic review and meta-analysis. JAMA Netw Open. 2019;2(11):e1915138.PubMedPubMedCentral Gomes F, Baumgartner A, Bounoure L, Bally M, Deutz NE, Greenwald JL, et al. Association of nutritional support with clinical outcomes among medical inpatients who are malnourished or at nutritional risk an updated systematic review and meta-analysis. JAMA Netw Open. 2019;2(11):e1915138.PubMedPubMedCentral
44.
go back to reference Kayambu G, Boots R, Paratz J. Physical therapy for the critically ill in the ICU: a systematic review and meta-analysis. Crit Care Med. 2013;41(6):1543–54.PubMed Kayambu G, Boots R, Paratz J. Physical therapy for the critically ill in the ICU: a systematic review and meta-analysis. Crit Care Med. 2013;41(6):1543–54.PubMed
45.
go back to reference Kollef MH, Shapiro SD, Silver P, St John RE, Prentice D, Sauer S, et al. A randomized, controlled trial of protocol-directed versus physician-directed weaning from mechanical ventilation. Crit Care Med. 1997;25(4):567–74.PubMed Kollef MH, Shapiro SD, Silver P, St John RE, Prentice D, Sauer S, et al. A randomized, controlled trial of protocol-directed versus physician-directed weaning from mechanical ventilation. Crit Care Med. 1997;25(4):567–74.PubMed
46.
go back to reference Woo HY, Oh SY, Lee H, Ryu HG. Evaluation of the association between decreased skeletal muscle mass and extubation failure after long-term mechanical ventilation. Clin Nutr. 2020;39(9):2764–70.PubMed Woo HY, Oh SY, Lee H, Ryu HG. Evaluation of the association between decreased skeletal muscle mass and extubation failure after long-term mechanical ventilation. Clin Nutr. 2020;39(9):2764–70.PubMed
47.
go back to reference Veld LPMOH, van Rossum E, Kempen GIJM, de Vet HCW, Hajema K, Beurskens AJHM. Fried phenotype of frailty: cross-sectional comparison of three frailty stages on various health domains. BMC Geriatr. 2015;15:77. Veld LPMOH, van Rossum E, Kempen GIJM, de Vet HCW, Hajema K, Beurskens AJHM. Fried phenotype of frailty: cross-sectional comparison of three frailty stages on various health domains. BMC Geriatr. 2015;15:77.
48.
go back to reference Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146–56.PubMed Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146–56.PubMed
49.
go back to reference Xu H, Cupples LA, Stokes A, Liu CT. Association of obesity with mortality over 24 years of weight history: findings from the Framingham Heart Study. JAMA Netw Open. 2018;1(7):e184587.PubMedPubMedCentral Xu H, Cupples LA, Stokes A, Liu CT. Association of obesity with mortality over 24 years of weight history: findings from the Framingham Heart Study. JAMA Netw Open. 2018;1(7):e184587.PubMedPubMedCentral
50.
go back to reference Buchman TG, Simpson SQ, Sciarretta KL, Finne KP, Sowers N, Collier M, et al. Sepsis among medicare beneficiaries: 3. The methods, models, and forecasts of sepsis, 2012–2018. Crit Care Med. 2020;48(3):302–18.PubMedPubMedCentral Buchman TG, Simpson SQ, Sciarretta KL, Finne KP, Sowers N, Collier M, et al. Sepsis among medicare beneficiaries: 3. The methods, models, and forecasts of sepsis, 2012–2018. Crit Care Med. 2020;48(3):302–18.PubMedPubMedCentral
Metadata
Title
Long-term clinical outcomes in critically ill patients with sepsis and pre-existing low muscle mass: a retrospective cohort study
Authors
Nola Darden
Sonakshi Sharma
Xue Wu
Benjamin Mancini
Kunal Karamchandani
Anthony S. Bonavia
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Anesthesiology / Issue 1/2023
Electronic ISSN: 1471-2253
DOI
https://doi.org/10.1186/s12871-023-02274-y

Other articles of this Issue 1/2023

BMC Anesthesiology 1/2023 Go to the issue