Whey Protein, L-Leucine and Vitamin D Supplementation for Preserving Lean Mass during a Low-Calorie Diet in Sarcopenic Obese Women
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Inclusion Criteria
2.3. Patients
2.4. Anthropometric Assessment
2.5. Blood and Urine Chemistry
2.6. Dual-Energy X-Ray Absorptiometry Measurement
2.7. Muscular Strenght and Functional Tests
2.8. Dietary Intervention
2.9. Data Management and Statistical Methods
2.10. Ethical Aspects
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sammarco, R.; Marra, M.; Di Guglielmo, M.L.; Naccarato, M.; Contaldo, F.; Poggiogalle, E.; Donini, L.M.; Pasanisi, F. Evaluation of Hypocaloric Diet With Protein Supplementation in Middle-Aged Sarcopenic Obese Women: A Pilot Study. Obes. Facts 2017, 10, 160–167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cruz-Jentoft, A.J.; Baeyens, J.P.; Bauer, J.M.; Boirie, Y.; Cederholm, T.; Landi, F.; Martin, F.C.; Michel, J.P.; Rolland, Y.; Schneider, S.M.; et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010, 39, 412–423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirai, K.; Ookawara, S.; Morishita, Y. Sarcopenia and Physical Inactivity in Patients with Chronic Kidney Disease. Nephro-urol. Mon. 2016, 8, e37443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilson, D.; Jackson, T.; Sapey, E.; Lord, J.M. Frailty and sarcopenia: The potential role of an aged immune system. Ageing Res. Rev. 2017, 36, 1–10. [Google Scholar] [CrossRef]
- Khadilkar, S.S. Musculoskeletal Disorders and Menopause. J Obstet. Gynaecol. India 2019, 69, 99–103. [Google Scholar] [CrossRef] [Green Version]
- Agostini, D.; Zeppa Donati, S.; Lucertini, F.; Annibalini, G.; Gervasi, M.; Ferri Marini, C.; Piccoli, G.; Stocchi, V.; Barbieri, E.; Sestili, P. Muscle and Bone Health in Postmenopausal Women: Role of Protein and Vitamin D Supplementation Combined with Exercise Training. Nutrients 2018, 10, 1103. [Google Scholar] [CrossRef] [Green Version]
- 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] [Green Version]
- Narici, M.V.; Maffulli, N. Sarcopenia: Characteristics, mechanisms and functional significance. Br. Med. Bull. 2010, 95, 139–159. [Google Scholar] [CrossRef] [Green Version]
- Batsis, J.A.; Villareal, D.T. Sarcopenic obesity in older adults: Aetiology, epidemiology and treatment strategies. Nat. Rev. Endocrinol. 2018, 14, 513–537. [Google Scholar] [CrossRef]
- Stenholm, S.; Harris, T.B.; Rantanen, T.; Visser, M.; Kritchevsky, S.B.; Ferrucci, L. Sarcopenic obesity: Definition, cause and consequences. Curr. Opin. Clin. Nutr. Metab. Care 2008, 11, 693–700. [Google Scholar] [CrossRef] [Green Version]
- Choi, K.M. Sarcopenia and sarcopenic obesity. Korean J. Intern. Med. 2016, 31, 1054–1060. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson Stoklossa, C.A.; Sharma, A.M.; Forhan, M.; Siervo, M.; Padwal, R.S.; Prado, C.M. Prevalence of Sarcopenic Obesity in Adults with Class II/III Obesity Using Different Diagnostic Criteria. J. Nutr. Metab. 2017, 2017, 7307618. [Google Scholar] [CrossRef] [PubMed]
- Parrinello, E.; Donini, L.M. Obesità sarcopenica. L’Endocrinologo 2020, 21, 354–358. [Google Scholar] [CrossRef]
- Sørensen, M.B.; Rosenfalck, A.M.; Højgaard, L.; Ottesen, B. Obesity and sarcopenia after menopause are reversed by sex hormone replacement therapy. Obes. Res. 2001, 9, 622–626. [Google Scholar] [CrossRef] [Green Version]
- LARN. Nutrients and Energy Reference Intake for Italian Population, 4th ed.; Italian Society of Human Nutrition (SINU): Milan, Italy, 2012. [Google Scholar]
- Bauer, J.; Biolo, G.; Cederholm, T.; Cesari, M.; Cruz-Jentoft, A.J.; Morley, J.E.; Phillips, S.; Sieber, C.; Stehle, P.; Teta, D.; et al. Evidence-based recommendations for optimal dietary protein intake in older people: A position paper from the PROT-AGE Study Group. J. Am. Med. Dir. Assoc. 2013, 14, 542–559. [Google Scholar] [CrossRef]
- Ganapathy, A.; Nieves, J.W. Nutrition and Sarcopenia-What Do We Know? Nutrients 2020, 12, 1755. [Google Scholar] [CrossRef]
- Coelho-Júnior, H.J.; Milano-Teixeira, L.; Rodrigues, B.; Bacurau, R.; Marzetti, E.; Uchida, M. Relative Protein Intake and Physical Function in Older Adults: A Systematic Review and Meta-Analysis of Observational Studies. Nutrients 2018, 10, 1330. [Google Scholar] [CrossRef] [Green Version]
- Cruz, B.; Oliveira, A.; Viana, L.R.; Lopes-Aguiar, L.; Canevarolo, R.; Colombera, M.C.; Valentim, R.R.; Garcia-Fóssa, F.; de Sousa, L.M.; Castelucci, B.G.; et al. Leucine-Rich Diet Modulates the Metabolomic and Proteomic Profile of Skeletal Muscle during Cancer Cachexia. Cancers 2020, 12, 1880. [Google Scholar] [CrossRef]
- Borack, M.S.; Volpi, E. Efficacy and Safety of Leucine Supplementation in the Elderly. J. Nutr. 2016, 146, 2625S–2629S. [Google Scholar] [CrossRef] [Green Version]
- FDA. Food: Dietary Supplements [Cited 2015 Oct 8]. Available online: http://www.fda.gov/Food/DietarySupplements/ (accessed on 11 November 2021).
- Pencharz, P.B.; Elango, R.; Ball, R.O. Determination of the Tolerable Upper Intake Level of leucine in adult men. J. Nutr. 2012, 142, 2220S–2224S. [Google Scholar] [CrossRef] [Green Version]
- Xu, Z.-R.; Tan, Z.-J.; Zhang, Q.; Gui, Q.-F.; Yang, Y.-M. The effectiveness of leucine on muscle protein synthesis, lean body mass and leg lean mass accretion in older people: A systematic review and meta-analysis. Br. J. Nutr. 2015, 113, 25–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tessier, A.J.; Chevalier, S. An Update on Protein, Leucine, Omega-3 Fatty Acids, and Vitamin D in the Prevention and Treatment of Sarcopenia and Functional Decline. Nutrients 2018, 10, 1099. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Basciani, S.; Camajani, E.; Contini, S.; Persichetti, A.; Risi, R.; Bertoldi, L.; Strigari, L.; Prossomariti, G.; Watanabe, M.; Mariani, S.; et al. Very-Low-Calorie Ketogenic Diets with Whey, Vegetable, or Animal Protein in Patients With Obesity: A Randomized Pilot Study. J. Clin. Endocrinol. Metab. 2020, 105, dgaa336. [Google Scholar] [CrossRef] [PubMed]
- Cockcroft, D.W.; Gault, M.H. Prediction of creatinine clearance from serum creatinine. Nephron 1976, 16, 31–41. [Google Scholar] [CrossRef]
- Matthews, D.R.; Hosker, J.P.; Rudenski, A.S.; Naylor, B.A.; Treacher, D.F.; Turner, R.C. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28, 412–419. [Google Scholar] [CrossRef] [Green Version]
- Bonaccorsi, G.; Romani, A.; Cremonini, E.; Bergamini, C.M.; Castaldini, M.C.; Fila, E.; Hanau, S.; Massari, L.; Cervellati, C. Oxidative stress and menopause-related hot flashes may be independent events. Taiwan. J. Obstet. Gynecol. 2015, 54, 290–293. [Google Scholar] [CrossRef] [Green Version]
- Verlaan, S.; Maier, A.B.; Bauer, J.M.; Bautmans, I.; Brandt, K.; Donini, L.M.; Maggio, M.; McMurdo, M.E.T.; Mets, T.; Seal, C.; et al. Sufficient levels of 25-hydroxyvitamin D and protein intake required to increase muscle mass in sarcopenic older adults—The PROVIDE study. Clin. Nutr. 2018, 37, 551–557. [Google Scholar] [CrossRef]
- Lombardo, M.; Boaria, A.; Aulisa, G.; Padua, E.; Annino, G.; Pratesi, A.; Caprio, M.; Iellamo, F.; Bellia, A. Sarcopenic obesity: Etiology and lifestyle therapy. Eur. Rev. Med. Pharmacol. Sci. 2019, 23, 7152–7162. [Google Scholar] [CrossRef]
- Wang, M.; Tan, Y.; Shi, Y.; Wang, X.; Liao, Z.; Wei, P. Diabetes and Sarcopenic Obesity: Pathogenesis, Diagnosis, and Treatments. Front. Endocrinol. 2020, 11, 568. [Google Scholar] [CrossRef]
- Goisser, S.; Kemmler, W.; Porzel, S.; Volkert, D.; Sieber, C.C.; Bollheimer, L.C.; Freiberger, E. Sarcopenic obesity and complex interventions with nutrition and exercise in community-dwelling older persons--a narrative review. Clin. Interv. Aging 2015, 10, 1267–1282. [Google Scholar] [CrossRef] [Green Version]
- Trouwborst, I.; Verreijen, A.; Memelink, R.; Massanet, P.; Boirie, Y.; Weijs, P.; Tieland, M. Exercise and Nutrition Strategies to Counteract Sarcopenic Obesity. Nutrients 2018, 10, 605. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beaudart, C.; Dawson, A.; Shaw, S.C.; Harvey, N.C.; Kanis, J.A.; Binkley, N.; Reginster, J.Y.; Chapurlat, R.; Chan, D.C.; Bruyère, O.; et al. Nutrition and physical activity in the prevention and treatment of sarcopenia: Systematic review. Osteoporos. Int. 2017, 28, 1817–1833. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Robinson, S.M.; Reginster, J.Y.; Rizzoli, R.; Shaw, S.C.; Kanis, J.A.; Bautmans, I.; Bischoff-Ferrari, H.; Bruyère, O.; Cesari, M.; Dawson-Hughes, B.; et al. Does nutrition play a role in the prevention and management of sarcopenia? Clin. Nutr. 2018, 37, 1121–1132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yanai, H. Nutrition for Sarcopenia. J. Clin. Med. Res. 2015, 7, 926–931. [Google Scholar] [CrossRef] [Green Version]
- Baum, J.I.; Kim, I.Y.; Wolfe, R.R. Protein Consumption and the Elderly: What Is the Optimal Level of Intake? Nutrients 2016, 8, 359. [Google Scholar] [CrossRef] [Green Version]
- Houston, D.K.; Nicklas, B.J.; Ding, J.; Harris, T.B.; Tylavsky, F.A.; Newman, A.B.; Lee, J.S.; Sahyoun, N.R.; Visser, M.; Kritchevsky, S.B.; et al. Dietary protein intake is associated with lean mass change in older, community-dwelling adults: The Health, Aging, and Body Composition (Health ABC) Study. Am. J. Clin. Nutr. 2008, 87, 150–155. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wall, B.T.; Hamer, H.M.; de Lange, A.; Kiskini, A.; Groen, B.B.; Senden, J.M.; Gijsen, A.P.; Verdijk, L.B.; van Loon, L.J. Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men. Clin. Nutr. 2013, 32, 412–419. [Google Scholar] [CrossRef]
- 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]
- Bruci, A.; Tuccinardi, D.; Tozzi, R.; Balena, A.; Santucci, S.; Frontani, R.; Mariani, S.; Basciani, S.; Spera, G.; Gnessi, L.; et al. Very Low-Calorie Ketogenic Diet: A Safe and Effective Tool for Weight Loss in Patients With Obesity and Mild Kidney Failure. Nutrients 2020, 12, 333. [Google Scholar] [CrossRef] [Green Version]
- Yoshimura, Y.; Bise, T.; Shimazu, S.; Tanoue, M.; Tomioka, Y.; Araki, M.; Nishino, T.; Kuzuhara, A.; Takatsuki, F. Effects of a leucine-enriched amino acid supplement on muscle mass, muscle strength, and physical function in post-stroke patients with sarcopenia: A randomized controlled trial. Nutrition 2019, 58, 1–6. [Google Scholar] [CrossRef]
- Welch, A.A.; Kelaiditi, E.; Jennings, A.; Steves, C.J.; Spector, T.D.; MacGregor, A. Dietary Magnesium Is Positively Associated With Skeletal Muscle Power and Indices of Muscle Mass and May Attenuate the Association Between Circulating C-Reactive Protein and Muscle Mass in Women. J. Bone Miner. Res. 2016, 31, 317–325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Petermann-Rocha, F.; Chen, M.; Gray, S.R.; Ho, F.K.; Pell, J.P.; Celis-Morales, C. Factors associated with sarcopenia: A cross-sectional analysis using UK Biobank. Maturitas 2020, 133, 60–67. [Google Scholar] [CrossRef] [PubMed]
- Giallauria, F.; Cittadini, A.; Smart, N.A.; Vigorito, C. Resistance training and sarcopenia. Monaldi Arch. Chest Dis. 2016, 84, 738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Makanae, Y.; Fujita, S. Role of Exercise and Nutrition in the Prevention of Sarcopenia. J. Nutr. Sci. Vitaminol. 2015, 61, S125–S127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colaianni, G.; Cuscito, C.; Mongelli, T.; Pignataro, P.; Buccoliero, C.; Liu, P.; Lu, P.; Sartini, L.; Di Comite, M.; Mori, G.; et al. The myokine irisin increases cortical bone mass. Proc. Natl. Acad. Sci. USA 2015, 112, 12157–12162. [Google Scholar] [CrossRef] [Green Version]
T 0 | T 45 | p < 0.05 | |
---|---|---|---|
Weight (Kg) | 96.8 ± 12.9 | 91.3 ± 13.1 | 0.162 |
Body Mass Index (Kg/m2) | 37.6 ± 4.4 | 35.7 ± 4.2 | 0.044 * |
Waist Circumference (cm) | 107 ± 7.4 | 102.4 ± 7.3 | 0.042 * |
Thigh Circumference (cm) | 62.4 ± 2.8 | 60.4 ± 2.6 | 0.046 * |
Systolic Body Pressure (mmHg) | 127 ± 11 | 120 ± 11 | 0.066 |
Diastolic Body Pressure (mmHg) | 75 ± 7 | 70 ± 10 | 0.060 |
Fasting Glycemia (mg/dL) | 112 ± 23.9 | 105.4 ± 14.2 | 0.145 |
Fasting Insulin (μIU/mL) | 17.4 ± 7.7 | 10.4 ± 3.9 | 0.001 * |
HOMA Index | 4.8 ± 2.2 | 2.3 ± 1.1 | 0.001 * |
Hb1AC (%) | 5.96 ± 0.6 | 5.67 ± 0.3 | 0.053 |
BUN (mg/dL) | 36.1 ± 7.8 | 46.3 ± 18.5 | 0.026 * |
Creatinine (mg/dL) | 0.79 ± 0.2 | 0.86 ± 0.2 | 0.192 |
eGFR | 124.2 ± 36.2 | 110.2 ± 37.2 | 0.140 |
Na (mmol/L) | 142.1 ± 2.1 | 140.7 ± 2 | 0.030 * |
K (mmol/L) | 4.4 ± 0.3 | 4.5 ± 0.3 | 0.280 |
Cl (mmol/L) | 100 ± 1.7 | 99 ± 1.8 | 0.076 |
Ca (mg/dL) | 9.6 ± 0.4 | 9.7 ± 0.5 | 0.230 |
Mg (mg/dL) | 2.0 ± 0.1 | 2.2 ± 0.1 | 0.002 * |
P (mg/dL) | 3.5 ± 0.5 | 3.7 ± 0.4 | 0.100 |
AST (U/L) | 17.5 ± 5.4 | 19.5 ± 4.2 | 0.128 |
ALT (U/L) | 21.2 ± 12.6 | 23.2 ± 11.4 | 0.321 |
Total Cholesterol (mg/dL) | 224 ± 56 | 207 ± 47 | 0.177 |
LDL Cholesterol (mg/dL) | 140 ± 53 | 128 ± 47 | 0.243 |
HDL Cholesterol (mg/dL) | 57 ± 13 | 55 ± 11 | 0.294 |
Triglycerides (mg/dL) | 132 ± 39 | 120 ± 35 | 0.192 |
Uric acid (mg/dL) | 5.2 ± 1.4 | 5.3 ± 1.4 | 0.424 |
CRP (mcg/L) | 7686 ± 6509 | 5643 ± 4973 | 0.166 |
ESR (mm/h) | 36 ± 15 | 38 ± 18 | 0.412 |
T 0 | T 45 | p < 0.05 | |
---|---|---|---|
Left Arm Fat (%) | 53 ± 5.2 | 49 ± 5.5 | 0.022 * |
Left Arm Lean (%) | 43 ± 7.1 | 48 ± 4.9 | 0.013 * |
Left Arm Fat (g) | 3040 ± 806 | 2733 ± 805 | 0.145 |
Left Arm Lean (g) | 2015 ± 411 | 2199 ± 324 | 0.085 |
Right Arm Fat (%) | 49 ± 5.3 | 47 ± 5.5 | 0.115 |
Right Arm Lean (%) | 46 ± 4.7 | 49 ± 5.2 | 0.060 |
Right Arm Fat (g) | 2905 ± 763 | 2618 ± 726 | 0.142 |
Right Arm Lean (g) | 2197 ± 320 | 2166 ± 307 | 0.192 |
Left Leg Fat (%) | 44 ± 4.4 | 41 ± 4.5 | 0.077 |
Left Leg Lean (%) | 49 ± 13 | 56 ± 6 | 0.029 * |
Left Leg Fat (g) | 6886 ± 1719 | 5727 ± 1863 | 0.038 * |
Left Leg Lean (g) | 6967 ± 1206 | 7361 ± 1262 | 0.186 |
Right Leg Fat (%) | 43 ± 5 | 41 ± 4.7 | 0.196 |
Right Leg Lean (%) | 54 ± 4.9 | 56 ± 4.5 | 0.161 |
Right Leg Fat (g) | 6812 ± 1754 | 6291 ± 1702 | 0.200 |
Right Leg Lean (g) | 7488 ± 1243 | 7417 ± 1305 | 0.437 |
Trunk Fat (g) | 21064 ± 4187 | 18517 ± 4266 | 0.049 * |
Trunk lean (g) | 27872 ± 2871 | 27682 ± 3309 | 0.431 |
Trunk Fat (%) | 42 ± 3.9 | 39 ± 4.5 | 0.026 * |
Trunk lean (%) | 56 ± 3.8 | 59 ± 4.4 | 0.026 * |
Total Fat (g) | 41797 ± 7705 | 37513 ± 7706 | 0.063 |
Total Lean (g) | 53182 ± 5496 | 53020 ± 6088 | 0.468 |
Total Fat (%) | 42 ± 3.3 | 40 ± 3.2 | 0.016 * |
Total Lean (%) | 55 ± 3.2 | 57 ± 3.1 | 0.017 * |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Camajani, E.; Persichetti, A.; Watanabe, M.; Contini, S.; Vari, M.; Di Bernardo, S.; Faro, M.; Lubrano, C.; Gnessi, L.; Caprio, M.; et al. Whey Protein, L-Leucine and Vitamin D Supplementation for Preserving Lean Mass during a Low-Calorie Diet in Sarcopenic Obese Women. Nutrients 2022, 14, 1884. https://doi.org/10.3390/nu14091884
Camajani E, Persichetti A, Watanabe M, Contini S, Vari M, Di Bernardo S, Faro M, Lubrano C, Gnessi L, Caprio M, et al. Whey Protein, L-Leucine and Vitamin D Supplementation for Preserving Lean Mass during a Low-Calorie Diet in Sarcopenic Obese Women. Nutrients. 2022; 14(9):1884. https://doi.org/10.3390/nu14091884
Chicago/Turabian StyleCamajani, Elisabetta, Agnese Persichetti, Mikiko Watanabe, Savina Contini, Michaela Vari, Settimia Di Bernardo, Maria Faro, Carla Lubrano, Lucio Gnessi, Massimiliano Caprio, and et al. 2022. "Whey Protein, L-Leucine and Vitamin D Supplementation for Preserving Lean Mass during a Low-Calorie Diet in Sarcopenic Obese Women" Nutrients 14, no. 9: 1884. https://doi.org/10.3390/nu14091884
APA StyleCamajani, E., Persichetti, A., Watanabe, M., Contini, S., Vari, M., Di Bernardo, S., Faro, M., Lubrano, C., Gnessi, L., Caprio, M., & Basciani, S. (2022). Whey Protein, L-Leucine and Vitamin D Supplementation for Preserving Lean Mass during a Low-Calorie Diet in Sarcopenic Obese Women. Nutrients, 14(9), 1884. https://doi.org/10.3390/nu14091884