Temporal Degradation of Skeletal Muscle Quality on CT as a Prognostic Marker in Septic Shock
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design and Population
2.2. Data Collection and Definition of Variables
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
| SOFA | Sequential organ failure assessment |
| APCT | Abdominopelvic computed tomography |
| HU | Hounsfield Units |
| ED | Emergency Department |
| APACHE | Acute Physiology and Chronic Health Evaluation |
| SFA | Subcutaneous fat area |
| VFA | Visceral fat area |
| NAMA | Normal attenuation muscle area |
| LAMA | Low attenuation muscle area |
| IMATA | Intramuscular adipose tissue area |
| IQR | Interquartile range |
| OR | Odds ratio |
| CI | Confidence interval |
References
- Rudd, K.E.; Johnson, S.C.; Agesa, K.M.; Shackelford, K.A.; Tsoi, D.; Kievlan, D.R.; Colombara, D.V.; Ikuta, K.S.; Kissoon, N.; Finfer, S.; et al. Global, regional, and national sepsis incidence and mortality, 1990–2017: Analysis for the Global Burden of Disease Study. Lancet 2020, 395, 200–211. [Google Scholar] [CrossRef]
- Singer, M.; Deutschman, C.S.; Seymour, C.W.; Shankar-Hari, M.; Annane, D.; Bauer, M.; Bellomo, R.; Bernard, G.R.; Chiche, J.-D.; Coopersmith, C.M.; et al. The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA 2016, 315, 801–810. [Google Scholar] [CrossRef] [PubMed]
- Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyere, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019, 48, 601. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.J.; Seo, D.W.; Kang, J.; Huh, J.W.; Kim, K.W.; Kim, W.Y. Impact of Body Composition Status on 90-Day Mortality in Cancer Patients with Septic Shock: Sex Differences in the Skeletal Muscle Index. J. Clin. Med. 2019, 8, 1583. [Google Scholar] [CrossRef]
- Blauwhoff-Buskermolen, S.; Versteeg, K.S.; de van der Schueren, M.A.E.; den Braver, N.R.; Berkhof, J.; Langius, J.A.E.; Verheul, H.M.W. Loss of Muscle Mass During Chemotherapy Is Predictive for Poor Survival of Patients With Metastatic Colorectal Cancer. J. Clin. Oncol. 2016, 34, 1339–1344. [Google Scholar] [CrossRef] [PubMed]
- Allen, S.L.; Quinlan, J.I.; Dhaliwal, A.; Armstrong, M.J.; Elsharkawy, A.M.; Greig, C.A.; Lord, J.M.; Lavery, G.G.; Breen, L. Sarcopenia in chronic liver disease: Mechanisms and countermeasures. Am. J. Physiol. Liver Physiol. 2021, 320, G241–G257. [Google Scholar] [CrossRef]
- Ryan, E.; McNicholas, D.; Creavin, B.; Kelly, M.E.; Walsh, T.; Beddy, D. Sarcopenia and Inflammatory Bowel Disease: A Systematic Review. Inflamm. Bowel. Dis. 2019, 25, 67–73. [Google Scholar] [CrossRef]
- Roukhomovsky-Moretti, M.; Uberti, T.; Giai, J.; Cerro, V.; Crozon-Clauzel, J.; Duclos, A.; Girardot, T.; Grégoire, A.; Hernu, R.; Huriaux, L.; et al. Prognostic Role of Unmeasured Anions Determined by the Stewart Approach in Septic Shock: A Prospective Cohort Study. J. Transl. Crit. Care Med. 2024, 6, e23-00003. [Google Scholar] [CrossRef]
- Kaibori, M.; Ishizaki, M.; Iida, H.; Matsui, K.; Sakaguchi, T.; Inoue, K.; Mizuta, T.; Ide, Y.; Iwasaka, J.; Kimura, Y.; et al. Effect of Intramuscular Adipose Tissue Content on Prognosis in Patients Undergoing Hepatocellular Carcinoma Resection. J. Gastrointest. Surg. 2015, 19, 1315–1323. [Google Scholar] [CrossRef]
- Miljkovic, I.; Cauley, J.A.; Wang, P.Y.; Holton, K.F.; Lee, C.G.; Sheu, Y.; Barrett-Connor, E.; Hoffman, A.R.; Lewis, C.B.; Orwoll, E.S.; et al. Abdominal myosteatosis is independently associated with hyperinsulinemia and insulin resistance among older men without diabetes. Obesity 2013, 21, 2118–2125. [Google Scholar] [CrossRef]
- Kim, D.W.; Kim, K.W.; Ko, Y.; Park, T.; Khang, S.; Jeong, H.; Koo, K.; Lee, J.; Kim, H.-K.; Ha, J.; et al. Assessment of Myosteatosis on Computed Tomography by Automatic Generation of a Muscle Quality Map Using a Web-Based Toolkit: Feasibility Study. JMIR Med. Inf. 2020, 8, e23049. [Google Scholar] [CrossRef] [PubMed]
- Fujiwara, N.; Nakagawa, H.; Kudo, Y.; Tateishi, R.; Taguri, M.; Watadani, T.; Nakagomi, R.; Kondo, M.; Nakatsuka, T.; Minami, T.; et al. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J. Hepatol. 2015, 63, 131–140. [Google Scholar] [CrossRef] [PubMed]
- Hopkins, J.J.; Reif, R.L.; Bigam, D.L.; Baracos, V.E.; Eurich, D.T.; Sawyer, M.B. The Impact of Muscle and Adipose Tissue on Long-term Survival in Patients With Stage I to III Colorectal Cancer. Dis. Colon Rectum 2019, 62, 549–560. [Google Scholar] [CrossRef] [PubMed]
- Spooren, C.E.; Lodewick, T.M.; Beelen, E.M.; van Dijk, D.P.; Bours, M.J.; Haans, J.J.; Masclee, A.A.; Pierik, M.J.; Bakers, F.C.; Jonkers, D.M. The reproducibility of skeletal muscle signal intensity on routine magnetic resonance imaging in Crohn’s disease. J. Gastroenterol. Hepatol. 2020, 35, 1902–1908. [Google Scholar] [CrossRef]
- Lattanzi, B.; Nardelli, S.; Pigliacelli, A.; Di Cola, S.; Farcomeni, A.; D’aMbrosio, D.; Gioia, S.; Corradini, S.G.; Lucidi, C.; Mennini, G.; et al. The additive value of sarcopenia, myosteatosis and hepatic encephalopathy in the predictivity of model for end-stage liver disease. Dig. Liver Dis. 2019, 51, 1508–1512. [Google Scholar] [CrossRef]
- Rhodes, A.; Evans, L.E.; Alhazzani, W.; Levy, M.M.; Antonelli, M.; Ferrer, R.; Kumar, A.; Sevransky, J.E.; Sprung, C.L.; Nunnally, M.E.; et al. Surviving Sepsis Campaign: International Guidelines for Management of Sepsis and Septic Shock: 2016. Intensive Care Med. 2017, 43, 304–377. [Google Scholar] [CrossRef]
- Casserly, B.; Phillips, G.S.; Schorr, C.; Dellinger, R.P.; Townsend, S.R.; Osborn, T.M.; Reinhart, K.; Selvakumar, N.; Levy, M.M. Lactate measurements in sepsis-induced tissue hypoperfusion: Results from the Surviving Sepsis Campaign database. Crit. Care Med. 2015, 43, 567–573. [Google Scholar] [CrossRef]
- Ha, J.; Park, T.; Kim, H.-K.; Shin, Y.; Ko, Y.; Kim, D.W.; Sung, Y.S.; Lee, J.; Ham, S.J.; Khang, S.; et al. Development of a fully automatic deep learning system for L3 selection and body composition assessment on computed tomography. Sci. Rep. 2021, 11, 21656. [Google Scholar] [CrossRef]
- van Vugt, J.L.; Braak, R.R.C.v.D.; Lalmahomed, Z.S.; Vrijland, W.W.; Dekker, J.W.; Zimmerman, D.D.; Vles, W.J.; Coene, P.-P.L.; Ijzermans, J.N. Impact of low skeletal muscle mass and density on short and long-term outcome after resection of stage I-III colorectal cancer. Eur. J. Surg. Oncol. 2018, 44, 1354–1360. [Google Scholar] [CrossRef]
- Kroenke, C.H.; Prado, C.M.; Meyerhardt, J.A.; Weltzien, E.K.; Xiao, J.; Feliciano, E.M.C.; Caan, B.J. Muscle radiodensity and mortality in patients with colorectal cancer. Cancer 2018, 124, 3008–3015. [Google Scholar] [CrossRef]
- Stretch, C.; Aubin, J.-M.; Mickiewicz, B.; Leugner, D.; Al-Manasra, T.; Tobola, E.; Salazar, S.; Sutherland, F.R.; Ball, C.G.; Dixon, E.; et al. Sarcopenia and myosteatosis are accompanied by distinct biological profiles in patients with pancreatic and periampullary adenocarcinomas. PLoS ONE 2018, 13, e0196235. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.-S.; Ha, J.; Kim, Y.-J.; Ko, Y.; Park, T.; Kim, K.W.; Kim, W.Y. The Impact of Myosteatosis Percentage on Short-Term Mortality in Patients with Septic Shock. J. Clin. Med. 2022, 11, 3031. [Google Scholar] [CrossRef]
- Correa-De-Araujo, R.; Rossi, A.P.; Zamboni, M.; Addison, O.; Miljkovic, I.; Goodpaster, B. Editorial: Muscle Quality in Skeletal Muscle Function Deficit: Recent Advances and Potential Clinical and Therapeutic Implications. Front. Physiol. 2022, 13, 847883. [Google Scholar] [CrossRef] [PubMed]
- Addison, O.; Marcus, R.L.; Lastayo, P.C.; Ryan, A.S. Intermuscular fat: A review of the consequences and causes. Int. J. Endocrinol. 2014, 2014, 309570. [Google Scholar] [CrossRef]
- Goodpaster, B.H.; Thaete, F.L.; Kelley, D.E. Composition of skeletal muscle evaluated with computed tomography. Ann. N. Y. Acad. Sci. 2000, 904, 18–24. [Google Scholar] [CrossRef]
- Cuff, D.J.; Meneilly, G.S.; Martin, A.; Ignaszewski, A.; Tildesley, H.D.; Frohlich, J.J. Effective exercise modality to reduce insulin resistance in women with type 2 diabetes. Diabetes Care 2003, 26, 2977–2982. [Google Scholar] [CrossRef]
- Aleixo, G.F.P.; Shachar, S.S.; Nyrop, K.A.; Muss, H.B.; Malpica, L.; Williams, G.R. Myosteatosis and prognosis in cancer: Systematic review and meta-analysis. Crit. Rev. Oncol. Hematol. 2020, 145, 102839. [Google Scholar] [CrossRef]
- Goodpaster, B.H.; Thaete, F.L.; Kelley, D.E. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am. J. Clin. Nutr. 2000, 71, 885–892. [Google Scholar] [CrossRef]
- Goodpaster, B.H.; Krishnaswami, S.; Resnick, H.; Kelley, D.E.; Haggerty, C.; Harris, T.B.; Schwartz, A.V.; Kritchevsky, S.; Newman, A.B. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 2003, 26, 372–379. [Google Scholar] [CrossRef]
- Goodpaster, B.H.; Carlson, C.L.; Visser, M.; Kelley, D.E.; Scherzinger, A.; Harris, T.B.; Stamm, E.; Newman, A.B. Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study. J. Appl. Physiol. (1985) 2001, 90, 2157–2165. [Google Scholar] [CrossRef]
- Hamrick, M.W.; McGee-Lawrence, M.E.; Frechette, D.M. Fatty Infiltration of Skeletal Muscle: Mechanisms and Comparisons with Bone Marrow Adiposity. Front. Endocrinol. 2016, 7, 69. [Google Scholar] [CrossRef]
- Chang, D.; Joseph, D.J.; A Ebert, M.; A Galvão, D.; Taaffe, D.R.; Denham, J.W.; Newton, R.U.; A Spry, N. Effect of androgen deprivation therapy on muscle attenuation in men with prostate cancer. J. Med. Imaging. Radiat. Oncol. 2014, 58, 223–228. [Google Scholar] [CrossRef]
- Cree, M.G.; Paddon-Jones, D.; Newcomer, B.R.; Ronsen, O.; Aarsland, A.; Wolfe, R.R.; Ferrando, A. Twenty-eight-day bed rest with hypercortisolemia induces peripheral insulin resistance and increases intramuscular triglycerides. Metabolism 2010, 59, 703–710. [Google Scholar] [CrossRef]
- Yoshihara, I.; Kondo, Y.; Okamoto, K.; Tanaka, H. Sepsis-Associated Muscle Wasting: A Comprehensive Review from Bench to Bedside. Int. J. Mol. Sci. 2023, 24, 5040. [Google Scholar] [CrossRef]
- Chen, L.; Zhou, S.; Wang, C.; Qie, G.; Tai, Z.; Wang, F.; Ding, R.; Liu, G.; Liu, Y.; Bai, X.; et al. Efficacy of HA380 Hemoperfusion in the Treatment of Septic Shock. J. Transl. Crit. Care Med. 2024, 6, e24-00008. [Google Scholar] [CrossRef]
- Taaffe, D.R.; Cauley, J.A.; Danielson, M.; Nevitt, M.C.; Lang, T.F.; Bauer, D.C.; Harris, T.B. Race and sex effects on the association between muscle strength, soft tissue, and bone mineral density in healthy elders: The Health, Aging, and Body Composition Study. J. Bone Min. Res. 2001, 16, 1343–1352. [Google Scholar] [CrossRef]
- Filbin, M.R.; Thorsen, J.E.; Lynch, J.; Gillingham, T.D.; Pasakarnis, C.L.; Capp, R.; Shapiro, N.I.; Mooncai, T.; Hou, P.C.; Heldt, T.; et al. Challenges and Opportunities for Emergency Department Sepsis Screening at Triage. Sci. Rep. 2018, 8, 11059. [Google Scholar] [CrossRef]



| Characteristics | Total | Survivor | Non-Survivor | p |
|---|---|---|---|---|
| (n = 768) | (n = 630) | (n = 138) | ||
| Age, year | 66.0 (59.0–74.0) | 67.0 (59.0–74.0) | 65.0 (58.0–71.0) | 0.48 |
| Male | 473 (61.6) | 386 (61.3) | 87 (63.0) | 0.70 |
| Past illness | ||||
| HTN | 231 (30.1) | 186 (29.5) | 45 (32.6) | 0.47 |
| DM | 200 (26.0) | 166 (26.3) | 34 (24.6) | 0.68 |
| CAD | 73 (9.5) | 59 (9.4) | 14 (10.1) | 0.78 |
| Chronic pulmonary disease | 50 (6.5) | 38 (6.0) | 12 (8.7) | 0.25 |
| Malignancy | 413 (53.8) | 325 (51.6) | 88 (63.8) | <0.01 |
| Hematologic disorder | 46 (6.0) | 35 (5.6) | 11 (8.0) | 0.28 |
| CKD | 56 (7.3) | 47 (7.5) | 9 (6.5) | 0.70 |
| LC | 142 (18.5) | 112 (17.8) | 30 (21.7) | 0.28 |
| Site of infection | ||||
| Unknown | 74 (9.6) | 64 (10.2) | 10 (7.2) | 0.29 |
| Lung | 105 (13.7) | 76 (12.1) | 29 (21.0) | <0.01 |
| Urinary tract | 111 (14.5) | 92 (14.6) | 19 (13.8) | 0.80 |
| Gastrointestinal | 117 (15.2) | 89 (14.1) | 28 (20.3) | 0.07 |
| Hepato-biliary-pancreas | 333 (43.4) | 284 (45.1) | 49 (35.5) | 0.04 |
| Bloodstream | 32 (4.2) | 21 (3.3) | 11 (8.0) | 0.01 |
| Lactate level, mmol/L | 3.3 (1.8–5.6) | 3.0 (1.7–5.2) | 5.4 (2.9–8.5) | <0.01 |
| SOFA score | 7.0 (5.0–10.0) | 7.0 (5.0–9.0) | 10.0 (6.0–12.0) | <0.01 |
| APACHE score | 17.0 (13.0–22.0) | 16.0 (12.0–21.0) | 21.0 (17.0–27.5) | <0.01 |
| CT interval * | 325 (182–377) | 321 (174–380) | 330 (182–369) | 0.65 |
| Body Composition | Total | Survivors | Non-Survivors | p |
|---|---|---|---|---|
| (n = 768) | (n = 630) | (n = 138) | ||
| SFA, cm2 | ||||
| ED visit day | 96.2 (55.9–145.0) | 92.9 (59.8–147.3) | 92.2 (37.3–146.9) | 0.34 |
| Baseline * | 113.3 (75.5–159.2) | 101.5 (73.5–155.0) | 103.3 (65.6–185.8) | 0.31 |
| Difference ** | −13.2 (−39.0–9.2) | −7.2 (−33.6–14.6) | −15.7 (32.6–9.3) | <0.01 |
| VFA, cm2 | ||||
| ED visit day | 88.6 (51.7–139.3) | 92.3 (52.0–140.6) | 97.0 (67.9–142.7) | 0.79 |
| Baseline * | 94.9 (53.7–144.7) | 98.3 (57.0–150.3) | 108.1 (59.5–126.0) | 0.43 |
| Difference ** | −4.2 (−28.0–18.2) | −7.9 (−30.0–17.6) | −8.1 (−27.3–29.1) | 0.84 |
| SMA, cm2 | ||||
| ED visit day | 105.3 (90.3–123.9) | 105.9 (93.5–128.5) | 109.6 (87.4–117.1) | 0.44 |
| Baseline * | 113.4 (96.5–138.0) | 115.4 (99.9–139.1) | 113.1 (97.3–143.3) | 0.82 |
| Difference ** | −8.2 (−20.1–0.0) | −7.9 (−19.1–0.7) | −11.4 (−21.3–3.3) | 0.30 |
| LAMA, cm2 | ||||
| ED visit day | 46.9 (35.4–59.2) | 46.4 (34.2–59.0) | 55.0 (48.4–67.0) | <0.01 |
| Baseline * | 34.2 (26.7–44.5) | 37.3 (27.9–54.6) | 35.3 (27.6–47.2) | 0.16 |
| Difference ** | 11.1 (2.3–20.4) | 9.8 (1.7–18.8) | 20.8 (5.5–29.3) | <0.01 |
| NAMA, cm2 | ||||
| ED visit day | 56.8 (39.6–77.3) | 61.2 (41.7–78.6) | 48.4 (31.0–60.3) | <0.01 |
| Baseline * | 78.3 (59.7–101.9) | 80.8 (62.1–100.8) | 72.2 (54.1–108.3) | 0.76 |
| Difference ** | −19.7 (−35.2–−7.6) | −18.8 (−31.8–−5.3) | −26.0 (−45.9–−7.2) | <0.01 |
| IMATA, cm2 | ||||
| ED visit day | 14.9 (8.8–22.1) | 14.9 (8.7–20.5) | 14.3 (9.3–22.3) | 0.77 |
| Baseline * | 14.0 (9.1–19.9) | 13.9 (8.8–19.9) | 12.1 (8.7–18.3) | 0.16 |
| Difference ** | 0.6 (−3.3–5.1) | 0.5 (−3.1–4.4) | 3.3 (−1.6–8.2) | 0.84 |
| Variables | Univariate Analysis | Multivariate Analysis | ||||
|---|---|---|---|---|---|---|
| OR | 95% CI | p-Value | aOR | 95% CI | p-Value | |
| Underlying malignancy | 2.19 | 1.36–3.55 | <0.01 | 2.06 | 1.29–3.30 | <0.01 |
| Site of infection | ||||||
| Lung | 2.10 | 1.13–3.90 | 0.02 | 2.15 | 1.22–3.79 | <0.01 |
| Gastrointestinal | 1.27 | 0.68–2.37 | 0.45 | |||
| Hepato-biliary-pancreas | 0.86 | 0.50–1.47 | 0.58 | |||
| Bloodstream | 2.36 | 0.94–5.90 | 0.07 | 2.39 | 0.97–5.90 | 0.06 |
| Lactate level | 1.14 | 1.07–1.22 | <0.01 | 1.14 | 1.07–1.22 | <0.01 |
| SOFA score | 1.12 | 1.03–1.20 | <0.01 | 1.12 | 1.04–1.20 | <0.01 |
| APACHE score | 1.03 | 1.01–1.08 | 0.02 | 1.04 | 1.01–1.08 | 0.01 |
| Body composition area | ||||||
| SFA difference | 0.99 | 0.98–0.99 | <0.01 | 0.99 | 0.98–1.00 | 0.06 |
| ED visit day LAMA | 1.01 | 1.00–1.03 | 0.16 | |||
| LAMA difference | 1.02 | 1.00–1.04 | 0.07 | 1.03 | 1.01–1.04 | <0.01 |
| ED visit day NAMA | 0.99 | 0.98–0.99 | <0.01 | 0.99 | 0.98–1.00 | 0.06 |
| NAMA difference | 0.98 | 0.98–1.01 | 0.08 | 0.99 | 0.97–1.03 | 0.09 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2026 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license.
Share and Cite
Kim, J.-s.; Ha, J.; Kim, Y.-J.; Ko, Y.; Kim, K.W.; Kim, W.Y. Temporal Degradation of Skeletal Muscle Quality on CT as a Prognostic Marker in Septic Shock. Diagnostics 2026, 16, 247. https://doi.org/10.3390/diagnostics16020247
Kim J-s, Ha J, Kim Y-J, Ko Y, Kim KW, Kim WY. Temporal Degradation of Skeletal Muscle Quality on CT as a Prognostic Marker in Septic Shock. Diagnostics. 2026; 16(2):247. https://doi.org/10.3390/diagnostics16020247
Chicago/Turabian StyleKim, June-sung, Jiyeon Ha, Youn-Jung Kim, Yousun Ko, Kyung Won Kim, and Won Young Kim. 2026. "Temporal Degradation of Skeletal Muscle Quality on CT as a Prognostic Marker in Septic Shock" Diagnostics 16, no. 2: 247. https://doi.org/10.3390/diagnostics16020247
APA StyleKim, J.-s., Ha, J., Kim, Y.-J., Ko, Y., Kim, K. W., & Kim, W. Y. (2026). Temporal Degradation of Skeletal Muscle Quality on CT as a Prognostic Marker in Septic Shock. Diagnostics, 16(2), 247. https://doi.org/10.3390/diagnostics16020247

