Lipid Metabolism Disorders as Diagnostic Biosignatures in Sepsis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients
2.2. Analysis of ApoA-IV
2.3. Analysis of Cholesterol and TG
2.4. Statistical Analysis
3. Results
3.1. Plasma ApoA-IV, Triglyceride and Cholesterol Levels of Controls and SIRS/Sepsis Patients
3.2. Plasma ApoA-IV and Lipid Levels of SIRS/Sepsis Patients in Relation to Sex, Age and BMI
3.3. Plasma ApoA-IV and Lipid Levels of SIRS/Sepsis Patients in Relation to SIRS, Sepsis and Septic Shock
3.4. Plasma ApoA-IV and Lipid Levels of SIRS/Sepsis Patients in Respect to Preexisting Diseases and SARS-CoV-2 Infection
3.5. Plasma ApoA-IV and Lipid Levels in Respect to Vasopressor Therapy and Interventions
3.6. Plasma ApoA-IV, Lipids and Inflammation Markers
3.7. Plasma ApoA-IV and Lipids in Bacterial Infections
3.8. Plasma ApoA-IV, Lipids and Survival
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Olofsson, S.O.; Wiklund, O.; Boren, J. Apolipoproteins A-I and B: Biosynthesis, role in the development of atherosclerosis and targets for intervention against cardiovascular disease. Vasc. Health Risk Manag. 2007, 3, 491–502. [Google Scholar] [PubMed]
- Florea, G.; Tudorache, I.F.; Fuior, E.V.; Ionita, R.; Dumitrescu, M.; Fenyo, I.M.; Bivol, V.G.; Gafencu, A.V. Apolipoprotein A-II, a Player in Multiple Processes and Diseases. Biomedicines 2022, 10, 1578. [Google Scholar] [CrossRef]
- Khovidhunkit, W.; Kim, M.S.; Memon, R.A.; Shigenaga, J.K.; Moser, A.H.; Feingold, K.R.; Grunfeld, C. Effects of infection and inflammation on lipid and lipoprotein metabolism: Mechanisms and consequences to the host. J. Lipid Res. 2004, 45, 1169–1196. [Google Scholar] [CrossRef]
- Kowalska, K.; Sabatowska, Z.; Forycka, J.; Mlynarska, E.; Franczyk, B.; Rysz, J. The Influence of SARS-CoV-2 Infection on Lipid Metabolism-The Potential Use of Lipid-Lowering Agents in COVID-19 Management. Biomedicines 2022, 10, 2320. [Google Scholar] [CrossRef] [PubMed]
- Zhao, M.; Luo, Z.; He, H.; Shen, B.; Liang, J.; Zhang, J.; Ye, J.; Xu, Y.; Wang, Z.; Ye, D.; et al. Decreased Low-Density Lipoprotein Cholesterol Level Indicates Poor Prognosis of Severe and Critical COVID-19 Patients: A Retrospective, Single-Center Study. Front. Med. 2021, 8, 585851. [Google Scholar] [CrossRef] [PubMed]
- Barlage, S.; Gnewuch, C.; Liebisch, G.; Wolf, Z.; Audebert, F.X.; Gluck, T.; Frohlich, D.; Kramer, B.K.; Rothe, G.; Schmitz, G. Changes in HDL-associated apolipoproteins relate to mortality in human sepsis and correlate to monocyte and platelet activation. Intensive Care Med. 2009, 35, 1877–1885. [Google Scholar] [CrossRef] [PubMed]
- Hofmaenner, D.A.; Kleyman, A.; Press, A.; Bauer, M.; Singer, M. The Many Roles of Cholesterol in Sepsis: A Review. Am. J. Respir. Crit. Care Med. 2022, 205, 388–396. [Google Scholar] [CrossRef]
- Sharma, N.K.; Ferreira, B.L.; Tashima, A.K.; Brunialti, M.K.C.; Torquato, R.J.S.; Bafi, A.; Assuncao, M.; Azevedo, L.C.P.; Salomao, R. Lipid metabolism impairment in patients with sepsis secondary to hospital acquired pneumonia, a proteomic analysis. Clin. Proteomics 2019, 16, 29. [Google Scholar] [CrossRef]
- Barker, G.; Leeuwenburgh, C.; Brusko, T.; Moldawer, L.; Reddy, S.T.; Guirgis, F.W. Lipid and Lipoprotein Dysregulation in Sepsis: Clinical and Mechanistic Insights into Chronic Critical Illness. J. Clin. Med. 2021, 10, 1693. [Google Scholar] [CrossRef]
- Karakike, E.; Giamarellos-Bourboulis, E.J.; Kyprianou, M.; Fleischmann-Struzek, C.; Pletz, M.W.; Netea, M.G.; Reinhart, K.; Kyriazopoulou, E. Coronavirus Disease 2019 as Cause of Viral Sepsis: A Systematic Review and Meta-Analysis. Crit. Care Med. 2021, 49, 2042–2057. [Google Scholar] [CrossRef]
- Marques, M.O.; Abdo, A.; Silva, P.B.; Silva Junior, A.; Alves, L.B.O.; Costa, J.V.G.; Martin, J.; Bachour, P.; Baiocchi, O.C.G. Soluble CD137 as a potential biomarker for severe COVID-19. Immunol. Lett. 2022, 248, 119–122. [Google Scholar] [CrossRef]
- Begue, F.; Chemello, K.; Veeren, B.; Lortat-Jacob, B.; Tran-Dinh, A.; Zappella, N.; Snauwaert, A.; Robert, T.; Rondeau, P.; Lagrange-Xelot, M.; et al. Plasma Apolipoprotein Concentrations Are Highly Altered in Severe Intensive Care Unit COVID-19 Patients: Preliminary Results from the LIPICOR Cohort Study. Int. J. Mol. Sci. 2023, 24, 4605. [Google Scholar] [CrossRef]
- Feingold, K.R. The bidirectional interaction of COVID-19 infections and lipoproteins. Best Pract. Res. Clin. Endocrinol. Metab. 2023, 37, 101751. [Google Scholar] [CrossRef]
- Qu, J.; Ko, C.W.; Tso, P.; Bhargava, A. Apolipoprotein A-IV: A Multifunctional Protein Involved in Protection against Atherosclerosis and Diabetes. Cells 2019, 8, 319. [Google Scholar] [CrossRef] [PubMed]
- Kohan, A.B.; Wang, F.; Lo, C.M.; Liu, M.; Tso, P. ApoA-IV: Current and emerging roles in intestinal lipid metabolism, glucose homeostasis, and satiety. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 308, G472–G481. [Google Scholar] [CrossRef] [PubMed]
- Dallongeville, J.; Lebel, P.; Parra, H.J.; Luc, G.; Fruchart, J.C. Postprandial lipaemia is associated with increased levels of apolipoprotein A-IV in the triacylglycerol-rich fraction and decreased levels in the denser plasma fractions. Br. J. Nutr. 1997, 77, 213–223. [Google Scholar] [CrossRef]
- Seishima, M.; Noma, A.; Torizawa, H.; Muto, Y. Changes of serum apolipoprotein levels after oral administration of fat in human subjects. Atherosclerosis 1988, 73, 39–43. [Google Scholar] [CrossRef]
- Recalde, D.; Ostos, M.A.; Badell, E.; Garcia-Otin, A.L.; Pidoux, J.; Castro, G.; Zakin, M.M.; Scott-Algara, D. Human apolipoprotein A-IV reduces secretion of proinflammatory cytokines and atherosclerotic effects of a chronic infection mimicked by lipopolysaccharide. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 756–761. [Google Scholar] [CrossRef] [PubMed]
- Vowinkel, T.; Mori, M.; Krieglstein, C.F.; Russell, J.; Saijo, F.; Bharwani, S.; Turnage, R.H.; Davidson, W.S.; Tso, P.; Granger, D.N.; et al. Apolipoprotein A-IV inhibits experimental colitis. J. Clin. Investig. 2004, 114, 260–269. [Google Scholar] [CrossRef]
- Shearston, K.; Tan, J.T.M.; Cochran, B.J.; Rye, K.A. Inhibition of Vascular Inflammation by Apolipoprotein A-IV. Front. Cardiovasc. Med. 2022, 9, 901408. [Google Scholar] [CrossRef]
- Roula, D.; Theiler, A.; Luschnig, P.; Sturm, G.J.; Tomazic, P.V.; Marsche, G.; Heinemann, A.; Sturm, E.M. Apolipoprotein A-IV acts as an endogenous anti-inflammatory protein and is reduced in treatment-naive allergic patients and allergen-challenged mice. Allergy 2020, 75, 392–402. [Google Scholar] [CrossRef] [PubMed]
- Khovidhunkit, W.; Duchateau, P.N.; Medzihradszky, K.F.; Moser, A.H.; Naya-Vigne, J.; Shigenaga, J.K.; Kane, J.P.; Grunfeld, C.; Feingold, K.R. Apolipoproteins A-IV and A-V are acute-phase proteins in mouse HDL. Atherosclerosis 2004, 176, 37–44. [Google Scholar] [CrossRef]
- Shi, T.; Bai, J.; Yang, D.; Huang, L.; Fan, H.F.; Zhang, D.W.; Liu, T.; Lu, G. Identification of candidate biomarkers for severe adenovirus community-acquired pneumonia by proteomic approach. Heliyon 2022, 8, e10807. [Google Scholar] [CrossRef] [PubMed]
- Flannery, A.H.; Li, X.; Delozier, N.L.; Toto, R.D.; Moe, O.W.; Yee, J.; Neyra, J.A. Sepsis-Associated Acute Kidney Disease and Long-term Kidney Outcomes. Kidney Med. 2021, 3, 507–514.e1. [Google Scholar] [CrossRef]
- Kronenberg, F. Apolipoprotein L1 and apolipoprotein A-IV and their association with kidney function. Curr. Opin. Lipidol. 2017, 28, 39–45. [Google Scholar] [CrossRef]
- Lingenhel, A.; Lhotta, K.; Neyer, U.; Heid, I.M.; Rantner, B.; Kronenberg, M.F.; Konig, P.; von Eckardstein, A.; Schober, M.; Dieplinger, H.; et al. Role of the kidney in the metabolism of apolipoprotein A-IV: Influence of the type of proteinuria. J. Lipid Res. 2006, 47, 2071–2079. [Google Scholar] [CrossRef] [PubMed]
- Romanova, Y.; Laikov, A.; Markelova, M.; Khadiullina, R.; Makseev, A.; Hasanova, M.; Rizvanov, A.; Khaiboullina, S.; Salafutdinov, I. Proteomic Analysis of Human Serum from Patients with Chronic Kidney Disease. Biomolecules 2020, 10, 257. [Google Scholar] [CrossRef] [PubMed]
- Cheng, C.W.; Chang, C.C.; Chen, H.W.; Lin, C.Y.; Chen, J.S. Serum ApoA4 levels predicted the progression of renal impairment in T2DM. Eur. J. Clin. Investig. 2018, 48, e12937. [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]
- Bone, R.C. Sepsis, sepsis syndrome, and the systemic inflammatory response syndrome (SIRS). Gulliver in Laputa. JAMA 1995, 273, 155–156. [Google Scholar] [CrossRef]
- Bligh, E.G.; Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37, 911–917. [Google Scholar] [CrossRef] [PubMed]
- Peschel, G.; Grimm, J.; Muller, M.; Horing, M.; Krautbauer, S.; Weigand, K.; Liebisch, G.; Buechler, C. Sex-specific changes in triglyceride profiles in liver cirrhosis and hepatitis C virus infection. Lipids Health Dis. 2022, 21, 106. [Google Scholar] [CrossRef]
- Horing, M.; Ejsing, C.S.; Krautbauer, S.; Ertl, V.M.; Burkhardt, R.; Liebisch, G. Accurate quantification of lipid species affected by isobaric overlap in Fourier-transform mass spectrometry. J. Lipid Res. 2021, 62, 100050. [Google Scholar] [CrossRef] [PubMed]
- Horing, M.; Ejsing, C.S.; Hermansson, M.; Liebisch, G. Quantification of Cholesterol and Cholesteryl Ester by Direct Flow Injection High-Resolution Fourier Transform Mass Spectrometry Utilizing Species-Specific Response Factors. Anal. Chem. 2019, 91, 3459–3466. [Google Scholar] [CrossRef]
- Hofmaenner, D.A.; Arina, P.; Kleyman, A.; Page Black, L.; Salomao, R.; Tanaka, S.; Guirgis, F.W.; Arulkumaran, N.; Singer, M. Association Between Hypocholesterolemia and Mortality in Critically Ill Patients with Sepsis: A Systematic Review and Meta-Analysis. Crit. Care Explor. 2023, 5, e0860. [Google Scholar] [CrossRef] [PubMed]
- Feingold, K.R.; Grunfeld, C. The Effect of Inflammation and Infection on Lipids and Lipoproteins. In Endotext; Feingold, K.R., Anawalt, B., Blackman, M.R., Boyce, A., Chrousos, G., Corpas, E., de Herder, W.W., Dhatariya, K., Dungan, K., Hofland, J., et al., Eds.; MDText.com, Inc.: South Dartmouth, MA, USA, 2000. [Google Scholar]
- Zhang, X.; Liu, H.; Hashimoto, K.; Yuan, S.; Zhang, J. The gut-liver axis in sepsis: Interaction mechanisms and therapeutic potential. Crit. Care 2022, 26, 213. [Google Scholar] [CrossRef]
- Li, X.; Xu, M.; Liu, M.; Ji, Y.; Li, Z. TNF-alpha and IL-6 inhibit apolipoprotein A-IV production induced by linoleic acid in human intestinal Caco2 cells. J. Inflamm. 2015, 12, 22. [Google Scholar] [CrossRef]
- Ghenu, M.I.; Dragos, D.; Manea, M.M.; Ionescu, D.; Negreanu, L. Pathophysiology of sepsis-induced cholestasis: A review. JGH Open 2022, 6, 378–387. [Google Scholar] [CrossRef]
- Sun, J.K.; Zhang, Q.; Shen, X.; Zhou, J.; Wang, X.; Zhou, S.M.; Mu, X.W. Integrin alphaEbeta7 is involved in the intestinal barrier injury of sepsis. Aging 2022, 14, 780–788. [Google Scholar] [CrossRef]
- Orso, E.; Moehle, C.; Boettcher, A.; Szakszon, K.; Werner, T.; Langmann, T.; Liebisch, G.; Buechler, C.; Ritter, M.; Kronenberg, F.; et al. The satiety factor apolipoprotein A-IV modulates intestinal epithelial permeability through its interaction with alpha-catenin: Implications for inflammatory bowel diseases. Horm. Metab. Res. 2007, 39, 601–611. [Google Scholar] [CrossRef]
- Peignon, G.; Thenet, S.; Schreider, C.; Fouquet, S.; Ribeiro, A.; Dussaulx, E.; Chambaz, J.; Cardot, P.; Pincon-Raymond, M.; Le Beyec, J. E-cadherin-dependent transcriptional control of apolipoprotein A-IV gene expression in intestinal epithelial cells: A role for the hepatic nuclear factor 4. J. Biol. Chem. 2006, 281, 3560–3568. [Google Scholar] [CrossRef]
- Buechler, C.; Aslanidis, C. Role of lipids in pathophysiology, diagnosis and therapy of hepatocellular carcinoma. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2020, 1865, 158658. [Google Scholar] [CrossRef] [PubMed]
- Wang, P.W.; Hung, Y.C.; Wu, T.H.; Chen, M.H.; Yeh, C.T.; Pan, T.L. Proteome-based identification of apolipoprotein A-IV as an early diagnostic biomarker in liver fibrosis. Oncotarget 2017, 8, 88951–88964. [Google Scholar] [CrossRef]
- Seishima, M.; Nishimuraa, M.; Moriwakib, H.; Mutob, Y.; Nomaa, A. Reduced intestinal apo A-IV mRNA levels in patients with liver cirrhosis. Int. Hepatol. Commun. 1995, 4, 153–159. [Google Scholar] [CrossRef]
- Reisinger, A.C.; Schuller, M.; Sourij, H.; Stadler, J.T.; Hackl, G.; Eller, P.; Marsche, G. Impact of Sepsis on High-Density Lipoprotein Metabolism. Front. Cell Dev. Biol. 2021, 9, 795460. [Google Scholar] [CrossRef] [PubMed]
- Taylor, R.; Zhang, C.; George, D.; Kotecha, S.; Abdelghaffar, M.; Forster, T.; Santos Rodrigues, P.D.; Reisinger, A.C.; White, D.; Hamilton, F.; et al. Low circulatory levels of total cholesterol, HDL-C and LDL-C are associated with death of patients with sepsis and critical illness: Systematic review, meta-analysis, and perspective of observational studies. eBioMedicine 2024, 100, 104981. [Google Scholar] [CrossRef] [PubMed]
- Massy, Z.A.; de Zeeuw, D. LDL cholesterol in CKD—To treat or not to treat? Kidney Int. 2013, 84, 451–456. [Google Scholar] [CrossRef]
- Sam, R.; Zhang, L.; Tuot, D.S.; Chaudhry, R. The Decrease in Serum Total Cholesterol and Low-Density Lipoprotein (LDL) Concentrations with the Initiation of Hemodialysis Despite a Concomitant Increase in Serum Albumin Concentrations. Cureus 2023, 15, e47272. [Google Scholar] [CrossRef]
- Stasi, A.; Franzin, R.; Fiorentino, M.; Squiccimarro, E.; Castellano, G.; Gesualdo, L. Multifaced Roles of HDL in Sepsis and SARS-CoV-2 Infection: Renal Implications. Int. J. Mol. Sci. 2021, 22, 5980. [Google Scholar] [CrossRef]
- Stangl, S.; Kollerits, B.; Lamina, C.; Meisinger, C.; Huth, C.; Stockl, A.; Dahnhardt, D.; Boger, C.A.; Kramer, B.K.; Peters, A.; et al. Association between apolipoprotein A-IV concentrations and chronic kidney disease in two large population-based cohorts: Results from the KORA studies. J. Intern. Med. 2015, 278, 410–423. [Google Scholar] [CrossRef]
- Holven, K.B.; Roeters van Lennep, J. Sex differences in lipids: A life course approach. Atherosclerosis 2023, 384, 117270. [Google Scholar] [CrossRef] [PubMed]
- Laclaustra, M.; Lopez-Garcia, E.; Civeira, F.; Garcia-Esquinas, E.; Graciani, A.; Guallar-Castillon, P.; Banegas, J.R.; Rodriguez-Artalejo, F. LDL Cholesterol Rises with BMI Only in Lean Individuals: Cross-sectional U.S. and Spanish Representative Data. Diabetes Care 2018, 41, 2195–2201. [Google Scholar] [CrossRef] [PubMed]
- Hussain, A.; Ali, I.; Kaleem, W.A.; Yasmeen, F. Correlation between Body Mass Index and Lipid Profile in patients with Type 2 Diabetes attending a tertiary care hospital in Peshawar. Pak. J. Med. Sci. 2019, 35, 591–597. [Google Scholar] [CrossRef] [PubMed]
- Verges, B.; Guerci, B.; Durlach, V.; Galland-Jos, C.; Paul, J.L.; Lagrost, L.; Gambert, P. Increased plasma apoA-IV level is a marker of abnormal postprandial lipemia: A study in normoponderal and obese subjects. J. Lipid Res. 2001, 42, 2021–2029. [Google Scholar] [CrossRef]
- Sun, Z.; Larson, I.A.; Ordovas, J.M.; Barnard, J.R.; Schaefer, E.J. Effects of age, gender, and lifestyle factors on plasma apolipoprotein A-IV concentrations. Atherosclerosis 2000, 151, 381–388. [Google Scholar] [CrossRef] [PubMed]
Parameters | Whole Cohort | Subcohort (Patients with Liver Cirrhosis Excluded) |
---|---|---|
Males/Females | 111/45 | 85/36 |
Age (years) | 59 (21–93) | 59 (21–93) |
BMI (kg/m2) | 27 (15–56) | 26 (15–56) |
C-reactive protein mg/L | 163 (4–697) | 183 (23–697) |
Procalcitonin ng/mL | 1.17 (0.05–270.00) | 1.12 (0.05–270.00) |
SIRS/Sepsis/Septic Shock | 39/39/78 | 26/31/64 |
IL-6 pg/mL | 89 (0–5702) 148 | 75 (0–5702) 117 |
Leukocytes n × 109/L | 10.31 (0.06–1586.00) | 10.24 (0.06–246.94) |
Neutrophils n/nL | 7.68 (0.01–70.20) | 7.34 (0–70.20) |
Basophils n/nL | 0.04 (0–0.90) | 0.04 (0–0.90) |
Eosinophils n/nL | 0.10 (0–8.80) | 0.13 (0–8.80) |
Monocytes n/nL | 0.75 (0–45.00) | 0.73 (0–4500) |
Lymphocytes n/nL | 0.95 (0.08 –28.60) | 1.07 (0.08–28.60) |
Immature granulocytes n/nL | 0.12 (0–6.19) | 0.13 (0–6.19) |
Aspartate aminotransferase U/L | 46 (6–1703) 143 | 40 (6–1597) 113 |
Alanine aminotransferase U/L | 32 (5–770) 141 | 32 (6–770) 111 |
Albumin g/L | 23.0 (6.3–42.0) 146 | 23.0 (6.3–42.0) 116 |
Gamma glutamyltransferase U/L | 124 (11–1266) 127 | 122 (11–1266) 100 |
Bilirubin mg/dL | 0.30 (0.10–7.80) 146 | 0.30 (0.10–4.60) 102 |
Intervention/Drug | ApoA-IV (ng/mL) | TG (µmol/mL) | CE (µmol/mL) | FC (µmol/mL) | ||||
---|---|---|---|---|---|---|---|---|
No | Yes | No | Yes | No | Yes | No | Yes | |
Dialysis (54/38) | 136 (63–273) | 151 (54–273) | 1.7 (0.2–15.4) | 1.5 (0.3–9.3) | 1.4 (0.1–3.7) | 0.9 (0.2–3.1) p = 0.002 | 1.2 (0.5–5.1) | 1.1 (0.4–4.2) |
Ventilation (93/75) | 141 (66–273) | 138 (54–273) | 1.5 (0.6–5.6) | 1.6 (0.2–15.4) | 1.3 (0.1–3.4) | 1.3 (0.2–3.7) | 1.1 (0.7–5.1) | 1.1 (0.4–4.2) |
Catecholamine (97/74) | 146 (66–273) | 135 (54–273) | 1.5 (0.3–5.4) | 1.6 (0.2–15.4) | 1.3 (0.1–3.4) | 1.2 (0.2–3.7) | 1.1 (0.6–5.1) | 1.1 (0.4–4.2) |
Biomarker of Inflammation | ApoA-IV | TG | CE | FC | ||||
---|---|---|---|---|---|---|---|---|
r | p-value | r | p-value | r | p-value | r | p-value | |
Leukocytes | −0.074 | 0.358 | 0.048 | 0.605 | −0.137 | 0.136 | 0.099 | 0.284 |
Neutrophils | −0.060 | 0.459 | 0.065 | 0.491 | −0.180 | 0.053 | 0.070 | 0.453 |
Basophils | 0.070 | 0.392 | 0.147 | 0.113 | −0.161 | 0.083 | 0.085 | 0.364 |
Eosinophils | 0.034 | 0.674 | 0.152 | 0.102 | −0.178 | 0.055 | 0.031 | 0.738 |
Monocytes | −0.007 | 0.927 | 0.075 | 0.421 | −0.227 | 0.014 | 0.012 | 0.899 |
Lymphocytes | −0.035 | 0.669 | 0.224 | 0.015 | −0.040 | 0.668 | 0.075 | 0.422 |
Immature granulocytes | −0.072 | 0.380 | 0.212 | 0.023 | −0.143 | 0.127 | 0.122 | 0.195 |
Procalcitonin | 0.094 | 0.250 | 0.120 | 0.198 | −0.364 | <0.001 | 0.174 | 0.061 |
C-reactive protein | −0.009 | 0.908 | 0.284 | 0.002 | −0.043 | 0.639 | 0.229 | 0.012 |
IL-6 | 0.076 | 0.361 | −0.065 | 0.487 | −0.267 | 0.004 | −0.080 | 0.391 |
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Birner, C.; Mester, P.; Liebisch, G.; Höring, M.; Schmid, S.; Müller, M.; Pavel, V.; Buechler, C. Lipid Metabolism Disorders as Diagnostic Biosignatures in Sepsis. Infect. Dis. Rep. 2024, 16, 806-819. https://doi.org/10.3390/idr16050062
Birner C, Mester P, Liebisch G, Höring M, Schmid S, Müller M, Pavel V, Buechler C. Lipid Metabolism Disorders as Diagnostic Biosignatures in Sepsis. Infectious Disease Reports. 2024; 16(5):806-819. https://doi.org/10.3390/idr16050062
Chicago/Turabian StyleBirner, Charlotte, Patricia Mester, Gerhard Liebisch, Marcus Höring, Stephan Schmid, Martina Müller, Vlad Pavel, and Christa Buechler. 2024. "Lipid Metabolism Disorders as Diagnostic Biosignatures in Sepsis" Infectious Disease Reports 16, no. 5: 806-819. https://doi.org/10.3390/idr16050062