Relationship Between Oral Intake and Sarcopenia in Patients with Disease-Related Malnutrition †
Abstract
1. Introduction
2. Materials and Methods
2.1. Type of Study
2.2. Study Population
2.3. Studied Parameters
- -
- BIA: (BIA NutriLab®; EFG Akern, Akern, Pisa, Italy) was performed between 8:00 and 9:15, after an overnight fast and after a time of 15 min in supine position. Resistance (R) and reactance (Xc) parameters were measured. The phase angle (PA) was calculated with: PA = ((Xc/R) × 180°/π) [22].
- -
- Muscle ultrasound of the RF of the dominant lower extremity was performed with a 10 to 12 MHz probe and a multifrequency linear array (Mindray Z60, Mindray Medical España S.L., Madrid, Spain). The measurement was performed with the patient in supine decubitus, without compression, at the level of the lower third from the superior pole of the patella and the anterosuperior iliac spine [15]. The measured parameters to assess muscle mass were anteroposterior (Y-axis) and transverse (X-axis) muscle thickness (cm), muscle area (RFMA, cm2). The variable used to assess muscle quality was the X-Y index ((X-axis/Y-axis)/height2) which relates transverse and anteroposterior muscle thickness.
2.4. Statistical Analysis
3. Results
3.1. Descriptive Analysis
3.2. Comparison Between Caloric and Protein Intake Higher and Lower than 70% for Nutritional Parameters
3.3. Correlation Between Caloric Intake and Nutritional Parameters
3.4. Assessment of Risk Factors for Sarcopenia
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Álvarez Hernández, J.P.M.V.; Planas Vila, M.; León-Sanz, M.; García de Lorenzo, A.; Celaya-Pérez, S.; García-Lorda, P.; Araujo, K.; Sarto Guerri, B.; on behalf of the PREDyCES® Researches. Prevalencia y costes de la malnutrición en pacientes hospitalizados; estudio predyces. Nutr. Hosp. 2012, 27, 1049–1059. [Google Scholar] [CrossRef] [PubMed]
- Merker, M.; Felder, M.; Gueissaz, L.; Bolliger, R.; Tribolet, P.; Kägi-Braun, N.; Gomes, F.; Hoess, C.; Pavlicek, V.; Bilz, S.; et al. Association of Baseline Inflammation with Effectiveness of Nutritional Support Among Patients with Disease-Related Malnutrition: A Secondary Analysis of a Randomized Clinical Trial. JAMA Netw. Open 2020, 3, e200663. [Google Scholar] [CrossRef]
- Cederholm, T.; Jensen, G.L.; Correia, M.I.T.D.; Gonzalez, M.C.; Fukushima, R.; Higashiguchi, T.; Baptista, G.; Barazzoni, R.; Blaauw, R.; Coats, A.J.S.; et al. GLIM criteria for the diagnosis of malnutrition—A consensus report from the global clinical nutrition community. Clin. Nutr. 2019, 38, 207–217. [Google Scholar] [CrossRef]
- 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]
- Meyer, F.; Valentini, L. Disease-Related Malnutrition and Sarcopenia as Determinants of Clinical Outcome. Visc. Med. 2019, 35, 282–291. [Google Scholar] [CrossRef] [PubMed]
- Park, B.; Bhat, S.; Xia, W.; Barazanchi, A.W.; Frampton, C.; Hill, A.G.; MacCormick, A.D. Consensus-defined sarcopenia predicts adverse outcomes after elective abdominal surgery: Meta-analysis. BJS Open 2023, 7, zrad065. [Google Scholar] [CrossRef] [PubMed]
- Chan, H.C.N.; Fei, X.; Leung, E.L.Y.; Langston, K.; Marshall, S.; van der Meij, B.S. Postdischarge consequences of protein-energy malnutrition, sarcopenia, and frailty in older adults admitted to rehabilitation: A systematic review. Clin. Nutr. ESPEN 2023, 54, 382–397. [Google Scholar] [CrossRef]
- Guillamón-Escudero, C.; Diago-Galmés, A.; Tenías-Burillo, J.M.; Soriano, J.M.; Fernández-Garrido, J.J. Prevalence of Sarcopenia in Community-Dwelling Older Adults in Valencia, Spain. Int. J. Environ. Res. Public Health 2020, 17, 9130. [Google Scholar] [CrossRef]
- Ethgen, O.; Beaudart, C.; Buckinx, F.; Bruyère, O.; Reginster, J.Y. The future prevalence of sarcopenia in Europe: A claim for public health action. Calcif. Tissue Int. 2017, 100, 229–234. [Google Scholar] [CrossRef]
- Gomes, F.; Schuetz, P.; Bounoure, L.; Austin, P.; Ballesteros-Pomar, M.; Cederholm, T.; Fletcher, J.; Laviano, A.; Norman, K.; Poulia, K.-A.; et al. ESPEN guidelines on nutritional support for polymorbid internal medicine patients. Clin Nutr. 2018, 37, 336–353. [Google Scholar] [CrossRef]
- Volkert, D.; Beck, A.M.; Cederholm, T.; Cruz-Jentoft, A.; Hooper, L.; Kiesswetter, E.; Maggio, M.; Raynaud-Simon, A.; Sieber, C.; Sobotka, L.; et al. ESPEN practical guideline: Clinical nutrition and hydration in geriatrics. Clin. Nutr. 2022, 41, 958–989. [Google Scholar] [CrossRef]
- Agarwal, E.; Ferguson, M.; Banks, M.; Batterham, M.; Bauer, J.; Capra, S.; Isenring, E. Malnutrition and poor food intake are associated with prolonged hospital stay, frequent readmissions, and greater in-hospital mortality: Results from the Nutrition Care Day Survey 2010. Clin. Nutr. 2013, 32, 737–745. [Google Scholar] [CrossRef] [PubMed]
- Cereda, E.; Pisati, R.; Rondanelli, M.; Caccialanza, R. Whey Protein, Leucine- and Vitamin-D-Enriched Oral Nutritional Supplementation for the Treatment of Sarcopenia. Nutrients 2022, 14, 1524. [Google Scholar] [CrossRef] [PubMed]
- García, C.G.; Almeida, J.M.G.; Aguilar, I.M.V.; Castañeda, V.B.; Guerrero, D.B. Morphofunctional assessment of patient nutritional status: A global approach. Nutr. Hosp. 2021, 38, 592–600. [Google Scholar] [CrossRef]
- García-Almeida, J.M.; García-García, C.; Ballesteros-Pomar, M.D.; Olveira, G.; Lopez-Gomez, J.J.; Bellido, V.; Lesmes, I.B.; Burgos, R.; Sanz-Paris, A.; Matia-Martin, P.; et al. Expert Consensus on Morphofunctional Assessment in Disease-Related Malnutrition. Grade Review and Delphi Study. Nutrients 2023, 15, 612. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Almeida, J.M. Nutritional ultrasound®: Conceptualisation, technical considerations and standardisation. Endocrinol. Diabetes Nutr. 2023, 70, 74–84. [Google Scholar] [CrossRef]
- López-Gómez, J.J.; Benito-Sendín Plaar, K.; Izaola-Jauregui, O.; Primo-Martín, D.; Gómez-Hoyos, E.; Torres-Torres, B.; De Luis-Román, D.A. Muscular Ultrasonography in Morphofunctional Assessment of Patients with Oncological Pathology at Risk of Malnutrition. Nutrients 2022, 14, 1573. [Google Scholar] [CrossRef]
- Barazzoni, R.; Jensen, G.L.; Correia, M.I.T.D.; Gonzalez, M.C.; Higashiguchi, T.; Shi, H.P.; Bischoff, S.C.; Boirie, Y.; Carrasco, F.; Cruz-Jentoft, A.; et al. Guidance for assessment of the muscle mass phenotypic criterion for the Global Leadership Initiative on Malnutrition (GLIM) diagnosis of malnutrition. Clin. Nutr. 2022, 41, 1425–1433. [Google Scholar] [CrossRef]
- Llames, L.; Baldomero, V.; Iglesias, M.L.; Rodota, L.P. Valores del ángulo de fase por bioimpedancia eléctrica; estado nutricional y valor pronóstico. Values of the phase angle by bioelectrical impedance; nutritional status and prognostic value. Nutr. Hosp. 2013, 28, 286–295. [Google Scholar] [CrossRef]
- Pérez-Mellen, I.; López-Andrés, E.; Villameriel Galván, M.J.; Castro Lozano, M.Á.; Izaola-Jáuregui, O.; Primo Martín, D.; Pérez-López, P.; Jiménez Sahagún, R.; López-Gómez, J.J.; de Luis Román, D. ¿Influye la ingesta dietética sobre la presencia de sarcopenia en el paciente con desnutrición relacionada con la enfermedad? In Proceedings of the 39th SENPE Congress, Palma de Mallorca, Spain, 15–17 May 2024. [Google Scholar]
- Pavlidou, E.; Papadopoulou, S.K.; Seroglou, K.; Giaginis, C. Revised Harris–Benedict Equation: New Human Resting Metabolic Rate Equation. Metabolites 2023, 13, 189. [Google Scholar] [CrossRef]
- Bellido, D.; García-García, C.; Talluri, A.; Lukaski, H.C.; García-Almeida, J.M. Future lines of research on phase angle: Strengths and limitations. Rev. Endocr. Metab. Disord. 2023, 24, 563–583. [Google Scholar] [CrossRef] [PubMed]
- Sergi, G.; De Rui, M.; Veronese, N.; Bolzetta, F.; Berton, L.; Carraro, S.; Bano, G.; Coin, A.; Manzato, E.; Perissinotto, E. Assessing appendicular skeletal muscle mass with bioelectrical impedance analysis in free-living Caucasian older adults. Clin. Nutr. 2015, 34, 667–673. [Google Scholar] [CrossRef]
- Otsuka, R.; Kato, Y.; Nishita, Y.; Tange, C.; Tomida, M.; Nakamoto, M.; Imai, T.; Ando, F.; Shimokata, H. Age-related Changes in Energy Intake and Weight in Community-dwelling Middle-aged and Elderly Japanese. J. Nutr. Health Aging 2016, 20, 383–390. [Google Scholar] [CrossRef] [PubMed]
- Calvani, R.; Picca, A.; Coelho-Júnior, H.J.; Tosato, M.; Marzetti, E.; Landi, F. Diet for the prevention and management of sarcopenia. Metabolism 2023, 146, 155637. [Google Scholar] [CrossRef]
- Hengeveld, L.M.; Boer, J.M.A.; Gaudreau, P.; Heymans, M.W.; Jagger, C.; Mendonça, N.; Ocké, M.C.; Presse, N.; Sette, S.; Simonsick, E.M.; et al. Prevalence of protein intake below recommended in community-dwelling older adults: A meta-analysis across cohorts from the PROMISS consortium. J. Cachexia Sarcopenia Muscle 2020, 11, 1212–1222. [Google Scholar] [CrossRef] [PubMed]
- Koh, F.H.-X.; Yik, V.; Chin, S.-E.; Kok, S.S.-X.; Lee, H.-B.; Tong, C.; Tay, P.; Chean, E.; Lam, Y.-E.; Mah, S.-M.; et al. Evaluating the Impact of Multimodal Prehabilitation with High Protein Oral Nutritional Supplementation (HP ONS) with Beta-Hydroxy Beta-Methylbutyrate (HMB) on Sarcopenic Surgical Patients—Interim Analysis of the HEROS Study. Nutrients 2024, 16, 4351. [Google Scholar] [CrossRef]
- Norman, K.; Stobäus, N.; Pirlich, M.; Bosy-Westphal, A. Phase angle and impedance vector analysis–clinical relevance and applicability of impedance parameters. Clin Nutr. 2012, 31, 854–861. [Google Scholar] [CrossRef]
n = 118 | SARCOPENIA | NO SARCOPENIA | p-Value |
---|---|---|---|
Patients | 50 (42%) | 68 (58%) | - |
Gender % (M/F) | 43.4/56.6 | 40/60 | p = 0.71 |
Age (years) | 70.4 (12.0) | 55.6 (17.7) | p < 0.01 |
Diabetes mellitus | 21 (39.6%) | 15 (23.1%) | p > 0.05 |
Oncologic (%) | 19 (35.8%) | 22 (33.8%) | p = 0.26 |
Autoimmune (%) | 9 (17.0%) | 10 (15.4%) | p = 0.26 |
Gastrointestinal (%) | 6 (11.3%) | 13 (20.0%) | p = 0.26 |
Body weight (kg) | 52.5 (10.2) | 57.0 (12.8) | p = 0.04 |
BMI (kg/m2) | 21.2 (21.2) | 21.8 (21.8) | p = 0.44 |
Dynamometry (kg) | 15.7 (6.1) | 25.4 (6.8) | p < 0.01 |
Resistance (ohm) | 606.8 (104.5) | 589.0 (106.6) | p = 0.37 |
Reactance (ohm) | 47.0 (9.0) | 54.1 (11.2) | p < 0.01 |
Phase Angle (°) | 4.5 (0.7) | 5.3 (0.8) | p < 0.01 |
X-axis (cm) | 3.4 (0.7) | 3.3 (0.7) | p = 0.44 |
Y-axis (cm) | 1.0 (0.5) | 1.2 (0.6) | p = 0.24 |
Y/X index | 0.3 (0.5) | 0.4 (0.5) | p = 0.24 |
RFMA (cm2) | 2.9 (1.2) | 3.3 (1.0) | p = 0.04 |
N = 114 | CAL < 70 | CAL > 70 | p-Value |
---|---|---|---|
Patients | 69 | 45 | - |
Gender % (M/F) | 57.8/42.2 | 29.6/70.4 | p = 0.28 |
Age (years) | 65.91 (14.10) | 59.94 (18.54) | p = 0.07 |
Body weight (kg) | 57.36 (12.67) | 53.43 (11.29) | p = 0.08 |
BMI (kg/m2) | 22.27 (3.88) | 21.08 (3.86) | p = 0.11 |
Dynamometry (kg) | 20.8 (7.4) | 21.4 (9.2) | p = 0.71 |
Resistance (ohm) | 618.8 (108.1) | 564.1 (93.7) | p < 0.01 |
Reactance (ohm) | 52.4 (11.4) | 48.8 (9.8) | p = 0.08 |
Phase Angle (°) | 4.9 (0.9) | 5.0 (0.8) | p = 0.50 |
X-axis (cm) | 3.3 (0.6) | 3.6 (0.9) | p = 0.74 |
Y-axis (cm) | 1.0 (0.4) | 1.2 (0.8) | p = 0.17 |
Y/X index | 0.3 (0.3) | 0.5 (0.8) | p = 0.22 |
RFMA (cm2) | 3.0 (1.2) | 3.2 (1.1) | p = 0.37 |
Sarcopenia (%) | 48.8 | 42.7 | p = 0.52 |
N = 106 | PROT < 70 | PROT > 70 | p-Value |
---|---|---|---|
Patients | 73 | 43 | - |
Age (years) | 57.13 (20.52) | 64.02 (15.30) | p = 0.05 |
Dynamometry (kg) | 20.9 (7.3) | 21.4 (9.4) | p = 0.79 |
Resistance (ohm) | 608.9 (104.1) | 576.3 (106.2) | p = 0.11 |
Reactance (ohm) | 52.4 (10.9) | 48.5 (10.5) | p = 0.06 |
Phase Angle (°) | 5.0 (0.9) | 4.8 (0.7) | p = 0.46 |
X-axis (cm) | 3.3 (0.7) | 3.3 (0.7) | p = 0.99 |
Y-axis (cm) | 1.1 (0.6) | 1.0 (0.4) | p = 0.15 |
Y/X index | 0.4 (0.6) | 0.3 (0.4) | p = 0.40 |
RFMA (cm2) | 3.2 (1.2) | 2.9 (1.0) | p = 0.33 |
Sarcopenia (%) | 54.8 | 41.4 | p = 0.19 |
N = 118 | p-Value | |
---|---|---|
BMI (kg/m2) | −0.228 | p < 0.01 |
Dynamometry (kg) | −0.041 | p = 0.09 |
Resistance (ohm) | 0.385 | p < 0.01 |
Reactance (ohm) | 0.327 | p < 0.01 |
Phase Angle (º) | 0.017 | p = 0.65 |
X-axis (cm) | −0.028 | p = 0.43 |
Y-axis (cm) | −0.005 | p = 0.82 |
Y/X index | −0.060 | p = 0.60 |
RFMA (cm2) | 0.019 | p = 0.13 |
OR | IC 95% | p-Value | |
---|---|---|---|
Age (years) | 1.07 | 1.04–1.11 | <0.01 |
Gender (M/F) | 0.48 | 0.55–3.55 | 0.48 |
Protein Intake (<70%) | 4.27 | 1.30–14.03 | 0.017 |
Caloric intake (<70%) | 1.33 | 0.53–3.31 | 0.77 |
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Pérez-López, P.; López-Gómez, J.J.; Izaola-Jauregui, O.; González-Gutiérrez, J.; Estévez-Asensio, L.; Pérez-Mellen, I.; López-Andrés, E.; Primo-Martín, D.; Delgado-García, E.; Jiménez-Sahagún, R.; et al. Relationship Between Oral Intake and Sarcopenia in Patients with Disease-Related Malnutrition. Nutrients 2025, 17, 2129. https://doi.org/10.3390/nu17132129
Pérez-López P, López-Gómez JJ, Izaola-Jauregui O, González-Gutiérrez J, Estévez-Asensio L, Pérez-Mellen I, López-Andrés E, Primo-Martín D, Delgado-García E, Jiménez-Sahagún R, et al. Relationship Between Oral Intake and Sarcopenia in Patients with Disease-Related Malnutrition. Nutrients. 2025; 17(13):2129. https://doi.org/10.3390/nu17132129
Chicago/Turabian StylePérez-López, Paloma, Juan José López-Gómez, Olatz Izaola-Jauregui, Jaime González-Gutiérrez, Lucía Estévez-Asensio, Isabel Pérez-Mellen, Eva López-Andrés, David Primo-Martín, Esther Delgado-García, Rebeca Jiménez-Sahagún, and et al. 2025. "Relationship Between Oral Intake and Sarcopenia in Patients with Disease-Related Malnutrition" Nutrients 17, no. 13: 2129. https://doi.org/10.3390/nu17132129
APA StylePérez-López, P., López-Gómez, J. J., Izaola-Jauregui, O., González-Gutiérrez, J., Estévez-Asensio, L., Pérez-Mellen, I., López-Andrés, E., Primo-Martín, D., Delgado-García, E., Jiménez-Sahagún, R., Ramos-Bachiller, B., & de Luis-Román, D. A. (2025). Relationship Between Oral Intake and Sarcopenia in Patients with Disease-Related Malnutrition. Nutrients, 17(13), 2129. https://doi.org/10.3390/nu17132129