Frailty and Sarcopenia Assessment in Patients with Advanced Chronic Liver Disease in a Tertiary Center in Romania
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Population Selection
2.2. Statistical Analysis
3. Results
3.1. Patients Characteristics
3.2. Short- and Long-Term Survival of Patients with Sarcopenia and Frailty
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bowers, S.P.; Brennan, P.N.; Dillon, J.F. Systematic review: The role of frailty in advanced chronic liver disease. Aliment. Pharmacol. Ther. 2023, 57, 280–289. [Google Scholar] [CrossRef]
- Wu, X.N.; Xue, F.; Zhang, N.; Zhang, W.; Hou, J.J.; Lv, Y.; Xiang, J.-X.; Zhang, X.-F. Global burden of liver cirrhosis and other chronic liver diseases caused by specific etiologies from 1990 to 2019. BMC Public Health 2024, 24, 363. [Google Scholar] [CrossRef] [PubMed]
- Cheemerla, S.; Balakrishnan, M. Global Epidemiology of Chronic Liver Disease. Clin. Liver Dis. 2021, 17, 365–370. [Google Scholar] [CrossRef] [PubMed]
- Trifan, A.; Muzica, C.M.; Nastasa, R.; Zenovia, S.; Stratina, E.; Stafie, R.; Rotaru, A.; Singeap, A.-M.; Cojocariu, C.; Sfarti, C.; et al. High prevalence of liver fibrosis among general population: A Romanian population-based study. Hepatol. Commun. 2023, 7, e0032. [Google Scholar] [CrossRef]
- Saraswat, V.A.; Kumar, K. Untangling the Web of Malnutrition, Sarcopenia, and Frailty in Chronic Liver Disease. J. Clin. Exp. Hepatol. 2022, 12, 268–271. [Google Scholar] [CrossRef] [PubMed]
- Mazeaud, S.; Zupo, R.; Couret, A.; Panza, F.; Sardone, R.; Castellana, F. Prevalence of Sarcopenia in Liver Cirrhosis: A Systematic Review and Meta-Analysis. Clin. Transl. Gastroenterol. 2023, 14, e00584. [Google Scholar] [CrossRef] [PubMed]
- Xie, R.; Jing, X.; Yang, C. The prevalence and characteristics of frailty in cirrhosis patients: A meta-analysis and systematic review. Front. Med. 2024, 11, 1353406. [Google Scholar] [CrossRef]
- Cuciureanu, D.; Filip, P.V.; Pop, C.S.; Diaconu, S.L. A short history of sarcopenia and frailty and their impact on advanced chronic liver disease. J. Med. Life 2024, 17, 660–664. [Google Scholar] [PubMed]
- Traub, J.; Reiss, L.; Aliwa, B.; Stadlbauer, V. Malnutrition in Patients with Liver Cirrhosis. Nutrients 2021, 13, 540. [Google Scholar] [CrossRef]
- Wang, C.W.; Feng, S.; Covinsky, K.E.; Hayssen, H.; Zhou, L.Q.; Yeh, B.M.; Lai, J.C. A Comparison of Muscle Function, Mass, and Quality in Liver Transplant Candidates: Results From the Functional Assessment in Liver Transplantation Study. Transplantation 2016, 100, 1692–1698. [Google Scholar] [CrossRef] [PubMed]
- Campos-Varela, I.; Castells, L.; Quiroga, S.; Vargas, V.; Simon-Talero, M. Frailty and sarcopenia in patients with acute-on-chronic liver failure: Assessment and risk in the liver transplant setting. Ann. Hepatol. 2024, 29, 101515. [Google Scholar] [CrossRef] [PubMed]
- Pellicoro, A.; Ramachandran, P.; Iredale, J.P.; Fallowfield, J.A. Liver fibrosis and repair: Immune regulation of wound healing in a solid organ. Nat. Rev. Immunol. 2014, 14, 181–194. [Google Scholar] [CrossRef] [PubMed]
- Peng, Y.; Qi, X.; Guo, X. Child–Pugh Versus MELD Score for the Assessment of Prognosis in Liver Cirrhosis. Medicine 2016, 95, e2877. [Google Scholar] [CrossRef] [PubMed]
- Angermayr, B.; Cejna, M.; Karnel, F.; Gschwantler, M.; Koenig, F.; Pidlich, J.; Mendel, H.; Pichler, L.; Wichlas, M.; Kreil, A.; et al. Child-Pugh versus MELD score in predicting survival in patients undergoing transjugular intrahepatic portosystemic shunt. Gut 2003, 52, 879–885. [Google Scholar] [CrossRef] [PubMed]
- Laube, R.; Wang, H.; Park, L.; Heyman, J.K.; Vidot, H.; Majumdar, A.; Strasser, S.I.; McCaughan, G.W.; Liu, K. Frailty in advanced liver disease. Liver Int. 2018, 38, 2117–2128. [Google Scholar] [CrossRef] [PubMed]
- Tandon, P.; Montano-Loza, A.J.; Lai, J.C.; Dasarathy, S.; Merli, M. Sarcopenia and frailty in decompensated cirrhosis. J. Hepatol. 2021, 75, S147–S162. [Google Scholar] [CrossRef]
- Nishikawa, H.; Yok, K.; Enomoto, H.; Iwata, Y.; Sakai, Y.; Kishino, K.; Shimono, Y.; Ikeda, N.; Takashima, T.; Aizawa, N.; et al. Sarcopenia and Frailty in Chronic Liver Damage: Common and Different Points. Vivo 2020, 34, 2549–2559. [Google Scholar] [CrossRef] [PubMed]
- Guo, G.; Li, C.; Hui, Y.; Mao, L.; Sun, M.; Li, Y.; Yang, W.; Wang, X.; Yu, Z.; Fan, X.; et al. Sarcopenia and frailty combined increases the risk of mortality in patients with decompensated cirrhosis. Ther. Adv. Chronic Dis. 2022, 13, 20406223221109651. [Google Scholar] [CrossRef]
- Buchard, B.; Boirie, Y.; Cassagnes, L.; Lamblin, G.; Coilly, A.; Abergel, A. Assessment of Malnutrition, Sarcopenia and Frailty in Patients with Cirrhosis: Which Tools Should We Use in Clinical Practice? Nutrients 2020, 12, 186. [Google Scholar] [CrossRef] [PubMed]
- Lai, J.C.; Tandon, P.; Bernal, W.; Tapper, E.B.; Ekong, U.; Dasarathy, S.; Carey, E.J. Malnutrition, Frailty, and Sarcopenia in Patients With Cirrhosis: 2021 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology 2021, 74, 1611–1644. [Google Scholar] [CrossRef]
- Pitter, J.G.; Zemplényi, A.; Babarczy, B.; Németh, B.; Kaló, Z.; Vokó, Z. Frailty prevalence in 42 European countries by age and gender: Development of the SHARE Frailty Atlas for Europe. GeroScience 2023, 46, 1807–1824. [Google Scholar] [CrossRef]
- Belarmino, G.; Torrinhas, R.S.; Magalhães, N.V.; Heymsfield, S.B.; Waitzberg, D.L. New anthropometric and biochemical models for estimating appendicular skeletal muscle mass in male patients with cirrhosis. Nutrition 2021, 84, 111083. [Google Scholar] [CrossRef]
- Merli, M.; Berzigotti, A.; Zelber-Sagi, S.; Dasarathy, S.; Montagnese, S.; Genton, L.; Plauth, M.; Parés, A. EASL Clinical Practice Guidelines on nutrition in chronic liver disease. J. Hepatol. 2019, 70, 172–193. [Google Scholar] [CrossRef] [PubMed]
- Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, 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, 16–31. [Google Scholar] [CrossRef] [PubMed]
- Cruz-Jentoft, A.J.; Sayer, A.A. Sarcopenia. Lancet 2019, 393, 2636–2646. [Google Scholar] [CrossRef]
- Deng, L.X.; Bischoff, K.E.; Kent, D.S.; O’Riordan, D.L.; Pantilat, S.Z.; Lai, J.C. Frailty is strongly associated with self-reported symptom burden among patients with cirrhosis. Eur. J. Gastroenterol. Hepatol. 2021, 33, e395–e400. [Google Scholar] [CrossRef]
- Tagliafico, A.S.; Bignotti, B.; Torri, L.; Rossi, F. Sarcopenia: How to measure, when and why. Radiol. Med. 2022, 127, 228–237. [Google Scholar] [CrossRef]
- Amini, B.; Boyle, S.P.; Boutin, R.D.; Lenchik, L. Approaches to Assessment of Muscle Mass and Myosteatosis on Computed Tomography: A Systematic Review. J. Gerontol. Ser. A 2019, 74, 1671–1678. [Google Scholar] [CrossRef]
- Dhaliwal, A.; Armstrong, M.J. Sarcopenia in cirrhosis: A practical overview. Clin. Med. 2020, 20, 489–492. [Google Scholar] [CrossRef] [PubMed]
- Tandon, P.; Tangri, N.; Thomas, L.; Zenith, L.; Shaikh, T.; Carbonneau, M.; Ma, M.; Bailey, R.J.; Jayakumar, S.; Burak, K.W.; et al. A Rapid Bedside Screen to Predict Unplanned Hospitalization and Death in Outpatients With Cirrhosis: A Prospective Evaluation of the Clinical Frailty Scale. Am. J. Gastroenterol. 2016, 111, 1759–1767. [Google Scholar] [CrossRef] [PubMed]
- McLean, C.; Ivers, R.; Antony, A.; McMahon, A.T. Malnutrition, nutritional deficiency and alcohol: A guide for general practice. Aust. J. Gen. Pract. 2024, 53, 173–178. [Google Scholar] [CrossRef]
With Sarcopenia + Frailty (n = 33) | Without Sarcopenia + with Frailty (n = 10) | Sarcopenia + Without Frailty (n = 24) | Without Sarcopenia + Frailty (n = 61) | p-Value | ||
---|---|---|---|---|---|---|
Age | 55.76 ± 10.46 (56.00) | 62.70 ± 9.673 (64.00) | 57.79 ± 11.54 (58.50) | 57.33 ± 12.83 (57.00) | 0.4464 | |
Gender | Female | 12 (36.36%) | 4 (40.00%) | 9 (37.50%) | 22 (36.07%) | 0.9956 |
Male | 21 (63.64%) | 6 (60.00%) | 15 (62.50%) | 39 (63.93%) | ||
Child–Pugh score | A | 3 (9.09%) | 1 (10.00%) | 7 (29.17%) | 29 (47.54%) | <0.0001 |
B | 7 (21.21%) | 3 (30.00%) | 11 (45.83%) | 20 (32.79%) | ||
C | 23 (69.70%) | 6 (60.00%) | 6 (25.00%) | 12 (19.67%) | ||
Child–Pugh scores values | 10.58 ± 2.550 (10.00) | 9.500 ± 2.014 (10.00) | 8.083 ± 1.692 (8.000) | 7.492 ± 1.988 (7.000) | <0.0001 | |
MELD-Na | 25.45 ± 6.924 (27.00) | 20.40 ± 5.680 (22.00) | 17.46 ± 4.433 (17.00) | 14.95 ± 5.640 (14.00) | <0.0001 | |
BMI | 25.01 ± 3.803 (24.92) | 23.57 ± 3.141 (23.83) | 25.17 ± 3.080 (25.19) | 25.28 ± 2.801 (25.18) | 0.4696 | |
HGS | 16.73 ± 4.869 (19.00) | 24.40 ± 7.961 (28.00) | 18.25 ± 5.194 (19.00) | 27.28 ± 5.905 (28.00) | <0.0001 | |
SMI | 40.20 ± 4.836 (41.98) | 49.04 ± 7.113 (52.19) | 42.15 ± 5.889 (43.99) | 49.77 ± 5.836 (51.26) | <0.0001 | |
LFI | 4.897 ± 0.267 (4.900) | 4.575 ± 0.099 (4.540) | 4.172 ± 0.219 (4.185) | 3.651 ± 0.368 (3.690) | <0.0001 | |
SPPB | 5.636 ± 1.496 (5.000) | 6.300 ± 1.767 (6.000) | 9.083 ± 1.349 (9.000) | 10.85 ± 1.621 (12.00) | <0.0001 | |
Albumin | 2.877 ± 0.480 (2.900) | 3.080 ± 0.547 (2.985) | 3.294 ± 0.398 (3.320) | 3.222 ± 0.542 (3.260) | 0.0060 | |
Natrium | 130.2 ± 5.758 (129.0) | 132.3 ± 3.945 (132.0) | 135.5 ± 4.061 (135.5) | 135.2 ± 3.459 (136.0) | <0.0001 | |
CRP | 13.46 ± 14.47 (9.800) | 10.65 ± 10.53 (7.750) | 7.401 ± 6.614 (6.240) | 6.788 ± 8.512 (4.200) | 0.0039 | |
Platelets | 78,848 ± 36,679 (67,000) | 90,400 ± 28,508 (97,000) | 110,000 ± 55,318 (102,500) | 115,623 ± 53,087 (102,000) | 0.0019 | |
Total bilirubin | 6.598 ± 6.466 (4.510) | 4.268 ± 4.179 (2.750) | 3.123 ± 2.601 (2.800) | 2.769 ± 3.129 (1.700) | <0.0001 | |
Encephalopathy | Present | 17 (51.52%) | 6 (60.00%) | 5 (20.83%) | 12 (19.67%) | 0.0017 |
Absent | 16 (48.48%) | 4 (40.00%) | 19 (79.17%) | 49 (80.33%) | ||
Refractor ascites | Present | 5 (15.15%) | 1 (10.00%) | 4 (16.67%) | 8 (13.11%) | 0.9506 |
Absent | 28 (84.85%) | 9 (90.00%) | 20 (83.33%) | 53 (86.89%) | ||
Pneumonia | Present | 8 (24.24%) | 1 (10.00%) | 2 (8.33%) | 7 (11.48%) | 0.2662 |
Absent | 25 (75.76%) | 9 (90.00%) | 22 (91.67%) | 54 (88.52%) | ||
UTI | Present | 11 (33.33%) | 3 (30.00%) | 5 (20.83%) | 11 (18.03%) | 0.3728 |
Absent | 22 (66.67%) | 7 (70.00%) | 19 (79.17%) | 50 (81.97%) | ||
SBP | Present | 11 (33.33%) | 3 (30.00%) | 5 (20.83%) | 6 (9.84%) | 0.0389 |
Absent | 22 (66.67%) | 7 (70.00%) | 19 (79.17%) | 55 (90.16%) | ||
Hospitalization days | 11.36 ± 10.38 (9.000) | 8.500 ± 2.799 (8.000) | 9.417 ± 4.180 (8.500) | 8.459 ± 3.134 (8.000) | 0.6389 | |
Re-admissions | 22 (66.67%) | 3 (30.00%) | 18 (75.00%) | 5 (8.20%) | <0.0001 | |
30-days readmissions | 16.82 ± 9.106 (16.50) | 22.67 ± 2.517 (23.00) | 23.44 ± 7.180 (26.00) | 24.20 ± 8.167 (27.00) | 0.0582 | |
In-hospital deaths | 9 (27.27%) | 1 (10.00%) | 0 (0.00%) | 3 (4.92%) | 0.0017 | |
180-day deaths | 27 (81.82%) | 2 (20.00%) | 4 (16.67%) | 7 (11.48%) | <0.0001 | |
12-month deaths | 33 (100.00%) | 9 (90.00%) | 19 (79.17%) | 13 (21.31%) | <0.0001 |
MELD-Na | |||
---|---|---|---|
Pearson r | 95% Confidence Interval | p-Value | |
HGS | −0.2354 | −0.3929 to −0.06444 | 0.0075 |
LFI | 0.6270 | 0.5088 to 0.7220 | <0.0001 |
All Four Groups | Univariable Analysis | Multivariable Analysis | ||||
---|---|---|---|---|---|---|
Estimate | 95% Confidence Interval | p-Value | Estimate | 95% Confidence Interval | p-Value | |
Age | −0.003 | −0.030 to 0.024 | 0.8314 | 0.020 | −0.013 to 0.053 | 0.2253 |
Gender | −0.033 | −0.700 to 0.635 | 0.9238 | |||
MELD-Na | 0.208 | 0.146 to 0.270 | <0.0001 | 0.192 | 0.087 to 0.297 | 0.0003 |
Child–Pugh | 0.480 | 0.316 to 0.644 | <0.0001 | 0.119 | −0.224 to 0.462 | 0.4961 |
Albumin | −0.950 | −1.600 to −0.301 | 0.0041 | 0.255 | −0.686 to 1.195 | 0.5957 |
Na | −0.185 | −0.262 to −0.107 | <0.0001 | |||
CRP | 0.055 | 0.017 to 0.094 | 0.0051 | 0.003 | −0.041 to 0.047 | 0.9024 |
Platelets | −1.203 × 103 | −1.940 × 103 to −4.668 × 103 | 0.0014 | |||
Bilirubin | 0.168 | 0.076 to 0.260 | 0.0004 | |||
Encephalopathy | 1.226 | 0.517 to 1.934 | 0.0007 | |||
Refractory ascites | 0.109 | −0.813 to 1.031 | 0.8175 | |||
Pneumonia | 0.710 | −0.207 to 1.627 | 0.1290 | −0.369 | −1.732 to 0.994 | 0.5959 |
UTI | 0.653 | −0.102 to 1.408 | 0.0900 | 0.0004 | −1.302 to 1.303 | 0.9994 |
SBP | 1.171 | 0.350 to 1.992 | 0.0052 | 0.269 | −0.656 to 1.957 | 0.5687 |
Four Groups | Univariable Analysis | ||
---|---|---|---|
Estimate | 95% Confidence Interval | p-Value | |
Alcohol | −0.145 | −0.790 to 0.500 | 0.6586 |
Viral | 0.294 | −0.398 to 0.986 | 0.4047 |
Metabolic | 0.532 | −0.600 to 1.664 | 0.3572 |
Autoimmune | −0.872 | −2.146 to 0.401 | 0.1794 |
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. |
© 2024 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Filip, P.V.; Cuciureanu, D.; Pop, C.S.; Marinescu, A.N.; Furtunescu, F.; Diaconu, L.S. Frailty and Sarcopenia Assessment in Patients with Advanced Chronic Liver Disease in a Tertiary Center in Romania. Diagnostics 2025, 15, 16. https://doi.org/10.3390/diagnostics15010016
Filip PV, Cuciureanu D, Pop CS, Marinescu AN, Furtunescu F, Diaconu LS. Frailty and Sarcopenia Assessment in Patients with Advanced Chronic Liver Disease in a Tertiary Center in Romania. Diagnostics. 2025; 15(1):16. https://doi.org/10.3390/diagnostics15010016
Chicago/Turabian StyleFilip, Petruta Violeta, Denisa Cuciureanu, Corina Silvia Pop, Andreea Nicoleta Marinescu, Florentina Furtunescu, and Laura Sorina Diaconu. 2025. "Frailty and Sarcopenia Assessment in Patients with Advanced Chronic Liver Disease in a Tertiary Center in Romania" Diagnostics 15, no. 1: 16. https://doi.org/10.3390/diagnostics15010016
APA StyleFilip, P. V., Cuciureanu, D., Pop, C. S., Marinescu, A. N., Furtunescu, F., & Diaconu, L. S. (2025). Frailty and Sarcopenia Assessment in Patients with Advanced Chronic Liver Disease in a Tertiary Center in Romania. Diagnostics, 15(1), 16. https://doi.org/10.3390/diagnostics15010016