Biomarker Changes in Response to a 12-Week Supplementation of an Oral Nutritional Supplement Enriched with Protein, Vitamin D and HMB in Malnourished Community Dwelling Older Adults with Sarcopenia
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Study Design
2.3. Statistical Analyses
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Vandewoude, M.F.J.; Alish, C.J.; Sauer, A.C.; Hegazi, R.A. Malnutrition-Sarcopenia Syndrome: Is This the Future of Nutrition Screening and Assessment for Older Adults? J. Aging Res. 2012, 2012, 651570. [Google Scholar] [CrossRef] [PubMed]
- Landi, F.; Camprubi-Robles, M.; Bear, D.; Cederholm, T.; Malafarina, V.; Welch, A.; Cruz-Jentoft, A. Muscle loss: The new malnutrition challenge in clinical practice. Clin. Nutr. 2018, 38, 2113–2120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jensen, G.L.; Cederholm, T.; Correia, M.I.T.; Fukushima, R.; Higashiguchi, T.; Baptista, G.A.; Barazzoni, R.; Blaauw, R.; Coats, A.J.; Crivelli, A.; et al. GLIM Criteria for the Diagnosis of Malnutrition: A Consensus Report from the Global Clinical Nutrition Community. J. Parenter. Enter. Nutr. 2018, 43, 32–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Landi, F.; Liperoti, R.; Russo, A.; Giovannini, S.; Tosato, M.; Capoluongo, E.; Bernabei, R.; Onder, G. Sarcopenia as a risk factor for falls in elderly individuals: Results from the ilSIRENTE study. Clin. Nutr. 2012, 31, 652–658. [Google Scholar] [CrossRef] [PubMed]
- Lumbers, M.; Driver, L.; Howland, R.; Older, M.; Williams, C. Nutritional status and clinical outcome in elderly femalesurgical orthopaedic patients. Clin. Nutr. 1996, 15, 101–107. [Google Scholar] [CrossRef]
- Vivanti, A.; Ward, N.; Haines, T. Nutritional status and associations with falls, balance, mobility and functionality during hospital admission. J. Nutr. Heal. Aging 2010, 15, 388–391. [Google Scholar] [CrossRef] [PubMed]
- Cederholm, T.; Jägren, C.; Hellström, K. Outcome of protein-energy malnutrition in elderly medical patients. Am. J. Med. 1995, 98, 67–74. [Google Scholar] [CrossRef]
- Cramer, J.T.; Cruz-Jentoft, A.J.; Landi, F.; Hickson, M.; Zamboni, M.; Pereira, S.L.; Hustead, D.S.; Mustad, V.A. Impacts of High-Protein Oral Nutritional Supplements Among Malnourished Men and Women with Sarcopenia: A Multicenter, Randomized, Double-Blinded, Controlled Trial. J. Am. Med. Dir. Assoc. 2016, 17, 1044–1055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bo, Y.; Liu, C.; Ji, Z.; Yang, R.; An, Q.; Zhang, X.; You, J.; Duan, D.; Sun, Y.; Zhu, Y.; et al. A high whey protein, vitamin D and E supplement preserves muscle mass, strength, and quality of life in sarcopenic older adults: A double-blind randomized controlled trial. Clin. Nutr. 2018, 38, 159–164. [Google Scholar] [CrossRef] [PubMed]
- Takeuchi, I.; Yoshimura, Y.; Shimazu, S.; Jeong, S.; Yamaga, M.; Koga, H. Effects of branched-chain amino acids and vitamin D supplementation on physical function, muscle mass and strength, and nutritional status in sarcopenic older adults undergoing hospital-based rehabilitation: A multicenter randomized controlled trial. Geriatr. Gerontol. Int. 2018, 19, 12–17. [Google Scholar] [CrossRef] [Green Version]
- Langsetmo, L.; Harrison, S.; Jonnalagadda, S.; Pereira, S.L.; Shikany, J.M.; Farsijani, S.; Lane, N.E.; Cauley, J.A.; Stone, K.; Cawthon, P.M.; et al. Low Protein Intake Irrespective of Source is Associated with Higher Mortality Among Older Community-Dwelling Men. J. Nutr. Heal. Aging 2020, 24, 900–905. [Google Scholar] [CrossRef] [PubMed]
- Coelho-Júnior, H.J.; Rodrigues, B.; Uchida, M.; Marzetti, E. Low Protein Intake Is Associated with Frailty in Older Adults: A Systematic Review and Meta-Analysis of Observational Studies. Nutrients 2018, 10, 1334. [Google Scholar] [CrossRef] [Green Version]
- Deutz, N.E.; Pereira, S.L.; Hays, N.P.; Oliver, J.S.; Edens, N.K.; Evans, C.M.; Wolfe, R.R. Effect of β-hydroxy-β-methylbutyrate (HMB) on lean body mass during 10 days of bed rest in older adults. Clin. Nutr. 2013, 32, 704–712. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Bischoff-Ferrari, H.A.; Dawson-Hughes, B.; Willett, W.C.; Staehelin, H.B.; Bazemore, M.G.; Zee, R.Y.; Wong, J.B. Effect of Vitamin D on Falls. JAMA 2004, 291, 1999–2006. [Google Scholar] [CrossRef] [PubMed]
- Garcia, M.; Seelaender, M.; Sotiropoulos, A.; Coletti, D.; Lancha, A.H. Vitamin D, muscle recovery, sarcopenia, cachexia, and muscle atrophy. Nutrition 2019, 60, 66–69. [Google Scholar] [CrossRef]
- Bruyère, O.; Cavalier, E.; Souberbielle, J.-C.; Bischoff-Ferrari, H.A.; Beaudart, C.; Buckinx, F.; Reginster, J.-Y.; Rizzoli, R. Effects of vitamin D in the elderly population: Current status and perspectives. Arch. Public Health 2014, 72, 32. [Google Scholar] [CrossRef] [Green Version]
- Bischoff-Ferrari, H. Vitamin D-why does it matter?—Defining vitamin D deficiency and its prevalence. Scand. J. Clin. Lab. Investig. Suppl. 2012, 243, 3–6. [Google Scholar] [CrossRef]
- Bear, D.E.; Langan, A.; Dimidi, E.; Wandrag, L.; Harridge, S.D.R.; Hart, N.; Connolly, B.; Whelan, K. β-Hydroxy-β-methylbutyrate and its impact on skeletal muscle mass and physical function in clinical practice: A systematic review and meta-analysis. Am. J. Clin. Nutr. 2019, 109, 1119–1132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stout, J.R.; Smith-Ryan, A.E.; Fukuda, D.H.; Kendall, K.L.; Moon, J.R.; Hoffman, J.R.; Wilson, J.M.; Oliver, J.S.; Mustad, V.A. Effect of calcium β-hydroxy-β-methylbutyrate (CaHMB) with and without resistance training in men and women 65+ yrs: A randomized, double-blind pilot trial. Exp. Gerontol. 2013, 48, 1303–1310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oktaviana, J.; Zanker, J.; Vogrin, S.; Duque, G. The Effect of β-Hydroxy-β-Methylbutyrate (HMB) on Sarcopenia and Functional Frailty in Older Persons: A Systematic Review. J. Nutr. Health Aging 2018, 23, 145–150. [Google Scholar] [CrossRef] [PubMed]
- Wilkinson, D.J.; Hossain, T.; Hill, D.S.; Phillips, B.; Crossland, H.; Williams, J.; Loughna, P.; Churchward-Venne, T.A.; Breen, L.; Phillips, S.; et al. Effects of leucine and its metabolite β-hydroxy-β-methylbutyrate on human skeletal muscle protein metabolism. J. Physiol. 2013, 591, 2911–2923. [Google Scholar] [CrossRef] [PubMed]
- Eley, H.L.; Russell, S.T.; Baxter, J.H.; Mukerji, P.; Tisdale, M.J. Signaling pathways initiated by β-hydroxy-β-methylbutyrate to attenuate the depression of protein synthesis in skeletal muscle in response to cachectic stimuli. Am. J. Physiol. Metab. 2007, 293, E923–E931. [Google Scholar] [CrossRef]
- Gerlinger-Romero, F.; Guimarães-Ferreira, L.; Giannocco, G.; Nunes, M. Chronic supplementation of beta-hydroxy-beta methylbutyrate (HMβ) increases the activity of the GH/IGF-I axis and induces hyperinsulinemia in rats. Growth Horm. IGF Res. 2011, 21, 57–62. [Google Scholar] [CrossRef] [PubMed]
- Smith, H.J.; Mukerji, P.; Tisdale, M.J. Attenuation of Proteasome-Induced Proteolysis in Skeletal Muscle by β-Hydroxy-β-Methylbutyrate in Cancer-Induced Muscle Loss. Cancer Res. 2005, 65, 277–283. [Google Scholar]
- Kovarik, M.; Muthny, T.; Sispera, L.; Holecek, M. Effects of β-hydroxy-β-methylbutyrate treatment in different types of skeletal muscle of intact and septic rats. J. Physiol. Biochem. 2010, 66, 311–319. [Google Scholar] [CrossRef]
- Girón, M.D.; Vilchez, J.D.; Shreeram, S.; Salto, R.; Manzano, M.; Cabrera, E.; Campos, N.; Edens, N.K.; Rueda, R.; López-Pedrosa, J.M. β-Hydroxy-β-Methylbutyrate (HMB) Normalizes Dexamethasone-Induced Autophagy-Lysosomal Pathway in Skeletal Muscle. PLoS ONE 2015, 10, e0117520. [Google Scholar] [CrossRef]
- Smith, H.J. Mechanism of the Attenuation of Proteolysis-Inducing Factor Stimulated Protein Degradation in Muscle by β-Hydroxy-β-Methylbutyrate. Cancer Res. 2004, 64, 8731–8735. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Integrated Care for Older People: Guidelines on Community-Level Interventions to Manage Declines in Intrinsic Capacity; WHO guidelines approved by the guidelines review committee; World Health Organization: Geneva, Switzerland, 2017; ISBN 978-92-4-155010-9. Available online: https://www.who.int/publications/i/item/9789241550109 (accessed on 1 March 2022).
- Sanz-Paris, A.; Camprubi-Robles, M.; Lopez-Pedrosa, J.M.; Pereira, S.L.; Rueda, R.; Ballesteros-Pomar, M.D.; Almeida, J.M.G.; Cruz-Jentoft, A.J. Role of Oral Nutritional Supplements Enriched with B-hydroxy-B-Methylbutyrate in Maintaining Muscle Function and Improving Clinical Outcomes in Various Clinical Settings. J. Nutr. Health Aging 2018, 22, 664–675. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chew, S.T.H.; Tan, N.C.; Cheong, M.; Oliver, J.; Baggs, G.; Choe, Y.; How, C.H.; Chow, W.L.; Tan, C.Y.L.; Kwan, S.C.; et al. Impact of specialized oral nutritional supplement on clinical, nutritional, and functional outcomes: A randomized, placebo-controlled trial in community-dwelling older adults at risk of malnutrition. Clin. Nutr. 2021, 40, 1879–1892. [Google Scholar] [CrossRef]
- Cornejo-Pareja, I.; Ramirez, M.; Camprubi-Robles, M.; Rueda, R.; Vegas-Aguilar, I.M.; Garcia-Almeida, J.M. Effect on an Oral Nutritional Supplement with β-Hydroxy-β-methylbutyrate and Vitamin D on Morphofunctional Aspects, Body Composition, and Phase Angle in Malnourished Patients. Nutrients 2021, 13, 4355. [Google Scholar] [CrossRef] [PubMed]
- Detsky, A.S.; McLaughlin, J.R.; Baker, J.P.; Johnston, N.; Whittaker, S.; Mendelson, R.A.; Jeejeebhoy, K.N. What is subjective global assessment of nutritional status? J. Parenter. Enter. Nutr. 1987, 11, 8–13. [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]
- Ingenbleek, Y.; De Visscher, M.; De Nayer, P. Measurement of prealbumin as index of protein-calorie malnutrition. Lancet 1972, 300, 106–109. [Google Scholar] [CrossRef]
- Ingenbleek, Y.; Schrieck, H.-G.V.D.; De Nayer, P.; De Visscher, M. Albumin, transferrin and the thyroxine-binding prealbumin/retinol-binding protein (TBPA-RBP) complex in assessment of malnutrition. Clin. Chim. Acta 1975, 63, 61–67. [Google Scholar] [CrossRef]
- Haspolat, K.; Ece, A.; Gürkan, F.; Atamer, Y.; Tutanç, M.; Yolbaş, I. Relationships between leptin, insulin, IGF-1 and IGFBP-3 in children with energy malnutrition. Clin. Biochem. 2007, 40, 201–205. [Google Scholar] [CrossRef]
- Gielen, E.; O’Neill, T.W.; Pye, S.R.; Adams, J.E.; Wu, F.C.; Laurent, M.R.; Claessens, F.; Ward, K.A.; Boonen, S.; Bouillon, R.; et al. Endocrine determinants of incident sarcopenia in middle-aged and elderly European men. J. Cachex. Sarcopenia Muscle 2015, 6, 242–252. [Google Scholar] [CrossRef] [Green Version]
- Ascenzi, F.; Barberi, L.; Dobrowolny, G.; Villa Nova Bacurau, A.; Nicoletti, C.; Rizzuto, E.; Rosenthal, N.; Scicchitano, B.M.; Musarò, A. Effects of IGF-1 isoforms on muscle growth and sarcopenia. Aging Cell 2019, 18, e12954. [Google Scholar] [CrossRef]
- Dong, J.; Zeng, Y.; Zhang, P.; Li, C.; Chen, Y.; Li, Y.; Wang, K. Serum IGFBP2 Level Is a New Candidate Biomarker of Severe Malnutrition in Advanced Lung Cancer. Nutr. Cancer 2019, 72, 858–863. [Google Scholar] [CrossRef]
- Matukumalli, S.R.; Tangirala, R.; Rao, C.M. Clusterin: Full-length protein and one of its chains show opposing effects on cellular lipid accumulation. Sci. Rep. 2017, 7, 41235. [Google Scholar] [CrossRef] [Green Version]
- Depper, J.M.; Leonard, W.J.; Drogula, C.; Kronke, M.; Waldmann, T.A.; Greene, W.C. Interleukin 2 (IL-2) augments transcription of the IL-2 receptor gene. Proc. Natl. Acad. Sci. USA 1985, 82, 4230–4234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- González-Martínez, H.; Rodríguez, L.; Nájera, O.; Cruz, D.; Miliar, A.; Domínguez, A.; Sánchez, F.; Graniel, J.; González-Torres, M.C. Expression of Cytokine mRNA in Lymphocytes of Malnourished Children. J. Clin. Immunol. 2008, 28, 593–599. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Zeng, F.; Forrester, S.J.; Eguchi, S.; Zhang, M.-Z.; Harris, R.C. Expression and Function of the Epidermal Growth Factor Receptor in Physiology and Disease. Physiol. Rev. 2016, 96, 1025–1069. [Google Scholar] [CrossRef] [PubMed]
- Zhu, M.; Qin, Y.-C.; Gao, C.-Q.; Yan, H.-C.; Wang, X.-Q. l-Glutamate drives porcine intestinal epithelial renewal by increasing stem cell activity via upregulation of the EGFR-ERK-mTORC1 pathway. Food Funct. 2020, 11, 2714–2724. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.-H.; Kuo, C.-H.; Shi, G.-Y.; Wu, H.-L. The role of thrombomodulin lectin-like domain in inflammation. J. Biomed. Sci. 2012, 19, 34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ricklin, D.; Reis, E.S.; Mastellos, D.C.; Gros, P.; Lambris, J.D. Complement component C3—The “Swiss Army Knife” of innate immunity and host defense. Immunol. Rev. 2016, 274, 33–58. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pilling, D.; Gomer, R.H. The Development of Serum Amyloid P as a Possible Therapeutic. Front. Immunol. 2018, 9, 2328. [Google Scholar] [CrossRef] [Green Version]
- Van Greevenbroek, M.M.J.; Arts, I.C.W.; Van Der Kallen, C.J.H.; Dagnelie, P.C.; Ferreira, I.; Jansen, E.; Schalkwijk, C.G.; Feskens, E.J.M.; Stehouwer, C.D.A. Complement C3 Is Inversely Associated with Habitual Intake of Provitamin A but Not with Dietary Fat, Fatty Acids, or Vitamin E in Middle-Aged to Older White Adults and Positively Associated with Intake of Retinol in Middle-Aged to Older White Women. J. Nutr. 2013, 144, 61–67. [Google Scholar] [CrossRef] [Green Version]
- Weber, M.-A.; Kinscherf, R.; Krakowski-Roosen, H.; Aulmann, M.; Renk, H.; Künkele, A.; Edler, L.; Kauczor, H.-U.; Hildebrandt, W. Myoglobin plasma level related to muscle mass and fiber composition—A clinical marker of muscle wasting? Klin. Wochenschr. 2007, 85, 887–896. [Google Scholar] [CrossRef]
- Pereira, S.; Davis, G.; Luo, M.; Gawel, S.; Chandran, R.; Deutz, N.; Wolfe, R.; Edens, N. LB010-sun β-HYDROXY-β-methylbutyrate (HMB) modulates circulating biomarkers in older adults on extended bedrest (BR). Clin. Nutr. 2013, 32, S226. [Google Scholar] [CrossRef]
- Maue, A.C.; Haynes, L. CD4+ T Cells and Immunosenescence—A Mini-Review. Gerontology 2009, 55, 491–495. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, S.; Busse, P.J. Innate and adaptive immunosenescence. Ann. Allergy Asthma Immunol. 2010, 104, 183–190. [Google Scholar] [CrossRef] [PubMed]
- Keilich, S.R.; Bartley, J.M.; Haynes, L. Diminished immune responses with aging predispose older adults to common and uncommon influenza complications. Cell. Immunol. 2019, 345, 103992. [Google Scholar] [CrossRef] [PubMed]
- Ibrahim, M.K.; Zambruni, M.; Melby, C.L.; Melby, P.C. Impact of Childhood Malnutrition on Host Defense and Infection. Clin. Microbiol. Rev. 2017, 30, 919–971. [Google Scholar] [CrossRef] [Green Version]
- Watson, R.R.; McMurray, D.N.; Martin, P.; Reyes, M.A. Effect of age, malnutrition and renutrition on free secretory component and IgA in secretions. Am. J. Clin. Nutr. 1985, 42, 281–288. [Google Scholar] [CrossRef] [Green Version]
- Reddy, V.; Raghuramulu, N.; Bhaskaram, C. Secretory IgA in protein-calorie malnutrition. Arch. Dis. Child 1976, 51, 871–874. [Google Scholar] [CrossRef] [Green Version]
- Charoenngam, N.; Holick, M.F. Immunologic Effects of Vitamin D on Human Health and Disease. Nutrients 2020, 12, 2097. [Google Scholar] [CrossRef]
- Wójcik, R.; Małaczewska, J.; Zwierzchowski, G.; Miciński, J.; Kaczorek-Łukowska, E. The influence of dietary supplementation with the leucine metabolite β-hydroxy-β-methylbutyrate (HMB) on the chemotaxis, phagocytosis and respiratory burst of peripheral blood granulocytes and monocytes in calves. BMC Veter. Res. 2020, 16, 171. [Google Scholar] [CrossRef]
- Peterson, A.L.; Qureshi, M.A.; Ferket, P.R.; Fuller, J.C. Enhancement of Cellular and Humoral Immunity in Young Broilers by the Dietary Supplementation of β-Hydroxy-β-Methylbutyrate. Immunopharmacol. Immunotoxicol. 1999, 21, 307–330. [Google Scholar] [CrossRef]
- Wójcik, R.; Ząbek, K.; Małaczewska, J.; Milewski, S.; Kaczorek-Łukowska, E. The Effects of β-Hydroxy-β-Methylbutyrate (HMB) on Chemotaxis, Phagocytosis, and Oxidative Burst of Peripheral Blood Granulocytes and Monocytes in Goats. Animals 2019, 9, 1031. [Google Scholar] [CrossRef] [Green Version]
- Matheson, E.; Luo, M.; Davis, G.; Baggs, G.; Nelson, J.; Pereira, S.; Hagazi, R.; Ahmed, N.; Steele, C.; Deutz, N. MON-P090: Effect of a Specialized Ons on Serum Markers of Nutrition and Inflammation in Hospitalized Malnourished Older Patients. Clin. Nutr. 2016, 35, S186. [Google Scholar] [CrossRef]
- Semba, R.D.; Blaum, C.; Guralnik, J.M.; Moncrief, D.T.; Ricks, M.O.; Fried, L.P. Carotenoid and vitamin E status are associated with indicators of sarcopenia among older women living in the community. Aging Clin. Exp. Res. 2003, 15, 482–487. [Google Scholar] [CrossRef] [PubMed]
- Dominguez, L.J.; Barbagallo, M.; Lauretani, F.; Bandinelli, S.; Bos, A.; Corsi, A.M.; Simonsick, E.M.; Ferrucci, L. Magnesium and Muscle Performance in Older Persons: The InCHIANTI Study. Am. J. Clin. Nutr. 2006, 84, 419–426. [Google Scholar] [CrossRef] [PubMed]
- Petermann-Rocha, F.; Gray, S.R.; Pell, J.P.; Celis-Morales, C.; Ho, F.K. Biomarkers Profile of People with Sarcopenia: A Cross-sectional Analysis from UK Biobank. J. Am. Med. Dir. Assoc. 2020, 21, 2017e1–2017e9. [Google Scholar] [CrossRef] [PubMed]
- Barrett-Connor, E.; Laughlin, G.A.; Li, H.; Nielson, C.M.; Wang, P.Y.; Dam, T.T.; Cauley, J.A.; Ensrud, K.E.; Stefanick, M.L.; Lau, E.; et al. The association of concurrent vitamin D and sex hormone deficiency with bone loss and fracture risk in older men: The osteoporotic fractures in men (MrOS) study. J. Bone Miner. Res. 2012, 27, 2306–2313. [Google Scholar] [CrossRef]
- Visser, M.; Pahor, M.; Taaffe, D.R.; Goodpaster, B.H.; Simonsick, E.M.; Newman, A.B.; Nevitt, M.; Harris, T.B. Relationship of Interleukin-6 and Tumor Necrosis Factor with Muscle Mass and Muscle Strength in Elderly Men and Women: The Health ABC Study. J. Gerontol. 2002, 57, M326–M332. [Google Scholar] [CrossRef] [Green Version]
- Rong, Y.-D.; Bian, A.-L.; Hu, H.-Y.; Ma, Y.; Zhou, X.-Z. Study on relationship between elderly sarcopenia and inflammatory cytokine IL-6, anti-inflammatory cytokine IL-10. BMC Geriatr. 2018, 18, 308. [Google Scholar] [CrossRef] [Green Version]
- Icer, M.A.; Gezmen-Karadag, M. The multiple functions and mechanisms of osteopontin. Clin. Biochem. 2018, 59, 17–24. [Google Scholar] [CrossRef] [PubMed]
- Karadag, F.; Gulen, S.T.; Karul, A.B.; Kilicarslan, N.; Ceylan, E.; Kuman, N.K.; Cildag, O. Osteopontin as a marker of weight loss in lung cancer. Scand. J. Clin. Lab. Investig. 2011, 71, 690–694. [Google Scholar] [CrossRef]
- Aparicio-Siegmund, S.; Garbers, Y.; Flynn, C.M.; Waetzig, G.H.; Gouni-Berthold, I.; Krone, W.; Berthold, H.K.; Laudes, M.; Rose-John, S.; Garbers, C. The IL-6-neutralizing sIL-6R-sgp130 buffer system is disturbed in patients with type 2 diabetes. Am. J. Physiol. Metab. 2019, 317, E411–E420. [Google Scholar] [CrossRef]
- Lustosa, L.P.; Batista, P.P.; Pereira, D.S.; Pereira, L.S.M.; Scianni, A.; Ribeiro-Samora, G.A. Comparison between parameters of muscle performance and inflammatory biomarkers of non-sarcopenic and sarcopenic elderly women. Clin. Interv. Aging 2017, 12, 1183–1191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Waetzig, G.H.; Rosenstiel, P.; Arlt, A.; Till, A.; Bräutigam, K.; Schäfer, H.; Rose-John, S.; Seegert, D.; Schreiber, S. Soluble tumor necrosis factor (TNF) receptor-1 induces apoptosis via reverse TNF signaling and autocrine transforming growth factor-β1. FASEB J. 2004, 19, 91–93. [Google Scholar] [CrossRef] [PubMed]
- Cankurtaran, M.; Yavuz, B.; Halil, M.; Ulger, Z.; Haznedaroğlu, I.; Arıoğul, S. Increased ferritin levels could reflect ongoing aging-associated inflammation and may obscure underlying iron deficiency in the geriatric population. Eur. Geriatr. Med. 2012, 3, 277–280. [Google Scholar] [CrossRef]
- Hoffman, J.R.; Gepner, Y.; Stout, J.R.; Hoffman, M.W.; Ben-Dov, D.; Funk, S.; Daimont, I.; Jajtner, A.R.; Townsend, J.R.; Church, D.D.; et al. β-Hydroxy-β-methylbutyrate attenuates cytokine response during sustained military training. Nutr. Res. 2016, 36, 553–563. [Google Scholar] [CrossRef]
- Gepner, Y.; Hoffman, J.R.; Shemesh, E.; Stout, J.R.; Church, D.D.; Varanoske, A.N.; Zelicha, H.; Shelef, I.; Chen, Y.; Frankel, H.; et al. Combined effect of Bacillus coagulans GBI-30, 6086 and HMB supplementation on muscle integrity and cytokine response during intense military training. J. Appl. Physiol. 2017, 123, 11–18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, S.-L.; Wu, J.; Zhu, L.; Chan, R.; Wang, X.; Huang, D.; Tang, N.; Woo, J. Peripheral Blood T Cell Gene Expression Responses to Exercise and HMB in Sarcopenia. Nutrients 2021, 13, 2313. [Google Scholar] [CrossRef]
Overall (n = 193) | EONS (n = 90) | CONS (n = 103) | p-Value c | ||
---|---|---|---|---|---|
Age (years) a | 77 (71, 81) | 77.5 (71, 82) | 76 (71, 81) | 0.308 | |
Sex b | Males | 75 (38.9%) | 36 (40.0%) | 39 (37.9%) | 0.761 |
Females | 118 (61.1%) | 54 (60.0%) | 64 (62.1%) | ||
Obese (kg·m−2) b | Obese ≥ 30 | 40 (20.7%) | 18 (20.0%) | 22 (21.4%) | 0.816 |
Non-Obese < 30 | 153 (79.3%) | 72 (80.0%) | 81 (78.6%) | ||
Body Mass Index a | 26.7 (23.5, 29.1) | 26.9 (23.1, 29.0) | 26.3 (23.9, 29.2) | 0.882 | |
<18.5 | Low b | 7 (3.6%) | 3 (3.3%) | 4 (3.9%) | 0.995 |
18.5–24.9 | Normal b | 62 (32.1%) | 29 (32.2%) | 33 (32.0%) | |
25.0–29.9 | Overweight b | 84 (43.5%) | 40 (44.4%) | 44 (42.7%) | |
≥30.0 | Obese b | 40 (20.7%) | 18 (20.0%) | 22 (21.4%) | |
Percent Total Lean Mass (%) a | 58.7 (54.3, 66.7) | 59.2 (55.3, 66.3) | 58.3 (53.5, 67.4) | 0.165 | |
Percent Leg Lean Mass (%) a | 30.4 (28.7, 32.0) | 30.4 (29.17, 32.0) | 30.4 (28.5, 32.0) | 0.846 | |
Handgrip Strength (kg) a | 18.8 (15.0, 27.3) | 19.2 (15.3, 29.3) | 18.7 (14.0, 26.0) | 0.285 | |
Low b | 141 (73.1%) | 60 (66.7%) | 81 (78.6%) | 0.061 | |
Normal b | 52 (26.9%) | 30 (33.3%) | 22 (21.4%) | ||
Male Handgrip Strength a | 27.8 (22.7, 34.7) | 29.6 (22.5, 34.7) | 26 (22.7, 33.0) | 0.411 | |
Low b | 45 (60.0%) | 19 (52.8%) | 26 (66.7%) | 0.220 | |
Normal b | 30 (40.0%) | 17 (47.2%) | 13 (33.3%) | ||
Female HandgripStrength a | 16.6 (13.2, 19.0) | 17 (14.0, 19.5) | 16.17 (12.7, 18.7) | 0.384 | |
Low b | 96 (81.4%) | 41 (75.9%) | 55 (85.9%) | 0.164 | |
Normal b | 22 (18.6%) | 13 (24.1%) | 9 (14.1%) | ||
Average Extensor Peak Torque (Nm) a | 58.7 (37.1, 78.3) | 58.8 (36.3, 79.2) | 58.7 (37.1, 78.3) | 0.753 | |
Peak Extensor Peak Torque (Nm) a | 62.2 (42.0, 82.0) | 62.2 (39.4, 81.1) | 62.9 (45.0, 82.7) | 0.841 | |
Gait Speed (m·s−1) b | Low | 115 (59.6%) | 57 (63.3%) | 58 (56.3%) | 0.321 |
Normal | 78 (40.4%) | 33 (36.7%) | 45 (43.7%) |
EONS (n = 90) a | CONS (n = 103) | |||||
---|---|---|---|---|---|---|
Biomarker | Baseline | 12 Weeks | Percent Change | Baseline | 12 Weeks | Percent Change |
Apolipoprotein(a) (Lp(a) (μg·mL−1) | 309.66 ± 305.59 | 388.60 ± 406.06 | 22.11 ± 31.72 c | 314.57 ± 356.34 | 339.66 ± 378.41 | 14.16 ± 36.51 b |
ApolipoproteinC III (Apo C-III) (μg·mL−1) | 229.32 ± 83.82 | 243.11 ± 80.41 | 8.60 ± 18.98 b | 229.01 ± 75.94 | 249.51 ± 82.57 | 10.49 ± 21.11 c |
Blood Urea Nitrogen (BUN) (mg·dL−1) | 18.71 ± 6.25 | 24.52 ± 9.31 | 33.86 ± 32.06 c | 19.37 ± 7.50 | 21.18 ± 7.73 | 13.29 ± 24.49 c |
Pre-Albumin (mg·dL−1) | 24.32 ± 5.27 | 25.60 ± 5.43 | 6.96 ± 16.15 b | 24.31 ± 5.20 | 25.69 ± 4.91 | 7.18 ± 15.17 c |
Transferrin (mg·dL−1) | 219.69 ± 42.68 | 239.10 ± 45.38 | 9.74 ± 13.47 c | 227.37 ± 48.57 | 241.74 ± 52.05 | 6.85 ± 11.51 c |
Vitamin B12 (mg·dL−1) | 593.76 ± 267.79 | 647.03 ± 273.07 | 14.80 ± 36.08 b | 529.26 ± 287.80 | 600.35 ± 293.74 | 21.27 ± 37.06 c |
Clusterin (μg·mL−1) | 215.67 ± 29.84 | 225.02 ± 31.48 | 4.81 ± 10.80 b | 209.23 ± 27.35 | 219.58 ± 29.63 | 5.47 ± 10.80 c |
Complement C3 (mg·mL−1) | 1.09 ± 0.21 | 1.15 ± 0.22 | 6.41 ± 15.50 b | 1.13 ± 0.22 | 1.20 ± 0.23 | 6.43 ± 11.85 c |
Epidermal Growth Factor Receptor (EGFR) (ng·mL−1) | 3.51 ± 0.55 | 3.83 ± 0.67 | 9.50 ± 11.80 c | 3.50 ± 0.53 | 3.68 ± 0.57 | 5.50 ± 10.42 c |
E-Selectin (ng·mL−1) | 8.65 ± 3.71 | 9.35 ± 3.70 | 9.89 ± 14.31 c | 9.67 ± 4.94 | 10.55 ± 4.83 | 10.89 ± 16.36 c |
Interluekin-2 Receptor Alpha (IL-2ra) (pg·mL−1) | 2582.33 ± 1590.01 | 2711.889 ± 1617.25 | 6.23 ± 14.94 b | 2554.37 ± 1094.80 | 2683.98 ± 1131.11 | 5.88 ± 14.65 b |
Serum Amyloid P-Component (SAP) (μg·mL−1) | 13.90 ± 4.22 | 15.07 ± 4.30 | 10.54 ± 18.43 c | 13.76 ± 3.65 | 15.20 ± 3.68 | 21.48 ± 17.56 c |
Thrombomodulin (ng·mL−1) | 5.51 ± 1.59 | 5.72 ± 1.49 | 4.91 ± 11.34 b | 5.70 ± 1.82 | 5.93 ± 1.83 | 4.72 ± 11.56 b |
Insulin-Like Growth Factor-1 (IGF-1) (ng·mL−1) | 1.76 ± 0.71 | 2.38 ± 1.01 | 46.96 ± 77.08 c | 1.73 ± 0.73 | 2.21 ± 0.96 | 38.39 ± 66.14 c |
Insulin-Like Growth Factor Binding Protein-2 (IGFBP-2) (ng·mL−1) | 170.47 ± 82.00 | 141.56 ± 74.81 | −15.44 ± 15.96 c | 151.26 ± 72.34 | 132.96 ± 71.96 | −11.13 ± 22.15 c |
Leptin (ng·mL−1) | 13.78 ± 10.71 | 18.76 ± 15.38 | 46.72 ± 55.73 c | 18.48 ± 20.44 | 24.20 ± 22.03 | 46.49 ± 53.02 c |
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
Pereira, S.L.; Shoemaker, M.E.; Gawel, S.; Davis, G.J.; Luo, M.; Mustad, V.A.; Cramer, J.T. Biomarker Changes in Response to a 12-Week Supplementation of an Oral Nutritional Supplement Enriched with Protein, Vitamin D and HMB in Malnourished Community Dwelling Older Adults with Sarcopenia. Nutrients 2022, 14, 1196. https://doi.org/10.3390/nu14061196
Pereira SL, Shoemaker ME, Gawel S, Davis GJ, Luo M, Mustad VA, Cramer JT. Biomarker Changes in Response to a 12-Week Supplementation of an Oral Nutritional Supplement Enriched with Protein, Vitamin D and HMB in Malnourished Community Dwelling Older Adults with Sarcopenia. Nutrients. 2022; 14(6):1196. https://doi.org/10.3390/nu14061196
Chicago/Turabian StylePereira, Suzette L., Marni E. Shoemaker, Susan Gawel, Gerard J. Davis, Menghua Luo, Vikkie A. Mustad, and Joel T. Cramer. 2022. "Biomarker Changes in Response to a 12-Week Supplementation of an Oral Nutritional Supplement Enriched with Protein, Vitamin D and HMB in Malnourished Community Dwelling Older Adults with Sarcopenia" Nutrients 14, no. 6: 1196. https://doi.org/10.3390/nu14061196
APA StylePereira, S. L., Shoemaker, M. E., Gawel, S., Davis, G. J., Luo, M., Mustad, V. A., & Cramer, J. T. (2022). Biomarker Changes in Response to a 12-Week Supplementation of an Oral Nutritional Supplement Enriched with Protein, Vitamin D and HMB in Malnourished Community Dwelling Older Adults with Sarcopenia. Nutrients, 14(6), 1196. https://doi.org/10.3390/nu14061196