Association of Dietary Protein Intake with Muscle Mass in Elderly Chinese: A Cross-Sectional Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data Source
2.2. Dietary Assessment
2.3. Outcome and Covariate Measurements
2.4. Statistical Analysis
3. Results
3.1. Participant Characteristics
3.2. Association between Dietary Protein Quantity, Quality, and Muscle Mass
3.3. Association between Dietary Protein Distribution and Muscle Mass
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- World Health Organization. Decade of Healthy Ageing: Baseline Report. Summary; World Health Organization: Geneva, Switzerland, 2021. [Google Scholar]
- National Bureau of Statistic. Available online: http://www.stats.gov.cn/tjsj/tjgb/rkpcgb/qgrkpcgb/202106/t20210628_1818824.html (accessed on 30 October 2022).
- van den Beld, A.W.; Kaufman, J.-M.; Zillikens, M.C.; Lamberts, S.W.J.; Egan, J.M.; Lely, A.J.v.d. The physiology of endocrine systems with ageing. Lancet Diabetes Endocrinol. 2018, 6, 647–658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sayer, A.A.; Syddall, H.; Martin, H.; Patel, H.; Baylis, D.; Cooper, C. The developmental origins of sarcopenia. J. Nutr. Health Aging 2008, 12, 427–432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.K.; Woo, J.; Assantachai, P.; Auyeung, T.W.; Chou, M.Y.; Iijima, K.; Jang, H.C.; Kang, L.; Kim, M.; Kim, S.; et al. Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J. Am. Med. Dir. Assoc. 2020, 21, 300–307.e2. [Google Scholar] [CrossRef] [PubMed]
- Anker, S.D.; Morley, J.E.; von Haehling, S. Welcome to the ICD-10 code for sarcopenia. J. Cachexia Sarcopenia Muscle 2016, 7, 512–514. [Google Scholar] [CrossRef] [PubMed]
- Distefano, G.; Goodpaster, B.H. Effects of Exercise and Aging on Skeletal Muscle. Cold. Spring. Harb. Perspect. Med. 2018, 8, a029785. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sahni, S.; Mangano, K.M.; Hannan, M.T.; Kiel, D.P.; McLean, R.R. Higher Protein Intake Is Associated with Higher Lean Mass and Quadriceps Muscle Strength in Adult Men and Women. J. Nutr. 2015, 145, 1569–1575. [Google Scholar] [CrossRef] [Green Version]
- Mendonça, N.; Hengeveld, L.M.; Visser, M. Low protein intake, physical activity, and physical function in European and North American community-dwelling older adults: A pooled analysis of four longitudinal aging cohorts. Am. J. Clin. Nutr. 2021, 114, 29–41. [Google Scholar] [CrossRef]
- Berryman, C.E.; Lieberman, H.R.; Fulgoni, V.L., 3rd; Pasiakos, S.M. Protein intake trends and conformity with the Dietary Reference Intakes in the United States: Analysis of the National Health and Nutrition Examination Survey, 2001–2014. Am. J. Clin. Nutr. 2018, 108, 405–413. [Google Scholar] [CrossRef] [Green Version]
- Gaytán-González, A.; Ocampo-Alfaro, M.J.; Torres-Naranjo, F.; González-Mendoza, R.G. Dietary Protein Intake Patterns and Inadequate Protein Intake in Older Adults from Four Countries. Nutrients 2020, 12, 3156. [Google Scholar] [CrossRef]
- Ouyang, Y.; Tan, T.; Song, X.; Huang, F. Dietary Protein Intake Dynamics in Elderly Chinese from 1991 to 2018. Nutrients 2021, 13, 3806. [Google Scholar] [CrossRef]
- Oliveira, C.L.P.; Dionne, I.J.; Prado, C.M. Are Canadian protein and physical activity guidelines optimal for sarcopenia prevention in older adults? Appl. Physiol. Nutr. Metab. 2018, 43, 1215–1223. [Google Scholar] [CrossRef] [PubMed]
- Lonnie, M.; Hooker, E.; Brunstrom, J.M.; Corfe, B.M.; Green, M.A.; Watson, A.W.; Williams, E.A.; Stevenson, E.J.; Penson, S.; Johnstone, A.M. Protein for Life: Review of Optimal Protein Intake, Sustainable Dietary Sources and the Effect on Appetite in Ageing Adults. Nutrients 2018, 10, 360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yoo, J.I.; Lee, K.H.; Choi, Y.; Lee, J.; Park, Y.G. Poor Dietary Protein Intake in Elderly Population with Sarcopenia and Osteosarcopenia: A Nationwide Population-Based Study. J. Bone Metab. 2020, 27, 301–310. [Google Scholar] [CrossRef] [PubMed]
- Bollwein, J.; Diekmann, R.; Kaiser, M.J.; Bauer, J.M.; Uter, W.; Sieber, C.C.; Volkert, D. Distribution but not amount of protein intake is associated with frailty: A cross-sectional investigation in the region of Nürnberg. Nutr. J. 2013, 12, 109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Loenneke, J.P.; Loprinzi, P.D.; Murphy, C.H.; Phillips, S.M. Per meal dose and frequency of protein consumption is associated with lean mass and muscle performance. Clin. Nutr. 2016, 35, 1506–1511. [Google Scholar] [CrossRef] [PubMed]
- Farsijani, S.; Morais, J.A.; Payette, H.; Gaudreau, P.; Shatenstein, B.; Gray-Donald, K.; Chevalier, S. Relation between mealtime distribution of protein intake and lean mass loss in free-living older adults of the NuAge study. Am. J. Clin. Nutr. 2016, 104, 694–703. [Google Scholar] [CrossRef] [Green Version]
- Farsijani, S.; Payette, H.; Morais, J.A.; Shatenstein, B.; Gaudreau, P.; Chevalier, S. Even mealtime distribution of protein intake is associated with greater muscle strength, but not with 3-y physical function decline, in free-living older adults: The Quebec longitudinal study on Nutrition as a Determinant of Successful Aging (NuAge study). Am. J. Clin. Nutr. 2017, 106, 113–124. [Google Scholar] [CrossRef] [Green Version]
- Mamerow, M.M.; Mettler, J.A.; English, K.L.; Casperson, S.L.; Arentson-Lantz, E.; Sheffield-Moore, M.; Layman, D.K.; Paddon-Jones, D. Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. J. Nutr. 2014, 144, 876–880. [Google Scholar] [CrossRef] [Green Version]
- Popkin, B.M.; Du, S.; Zhai, F.; Zhang, B. Cohort Profile: The China Health and Nutrition Survey--monitoring and understanding socio-economic and health change in China, 1989–2011. Int. J. Epidemiol. 2010, 39, 1435–1440. [Google Scholar] [CrossRef] [Green Version]
- Farsijani, S.; Cauley, J.A.; Santanasto, A.J.; Glynn, N.W.; Boudreau, R.M.; Newman, A.B. Transition to a More even Distribution of Daily Protein intake Is Associated with Enhanced Fat Loss during a Hypocaloric and Physical Activity Intervention in Obese Older Adults. J. Nutr. Health Aging 2020, 24, 210–217. [Google Scholar] [CrossRef]
- Ng, S.W.; Norton, E.C.; Popkin, B.M. Why have physical activity levels declined among Chinese adults? Findings from the 1991–2006 China Health and Nutrition Surveys. Soc. Sci. Med. 2009, 68, 1305–1314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ng, S.W.; Popkin, B.M. Time use and physical activity: A shift away from movement across the globe. Obes. Rev. 2012, 13, 659–680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alberti, K.G.; Zimmet, P.Z. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: Iagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 1998, 15, 539–553. [Google Scholar] [CrossRef]
- Li, C.W.; Yu, K.; Shyh-Chang, N.; Li, G.X.; Jiang, L.J.; Yu, S.L.; Xu, L.Y.; Liu, R.J.; Guo, Z.J.; Xie, H.Y.; et al. Circulating factors associated with sarcopenia during ageing and after intensive lifestyle intervention. J. Cachexia Sarcopenia Muscle 2019, 10, 586–600. [Google Scholar] [CrossRef] [Green Version]
- van Vliet, S.; Burd, N.A.; Loon, L.J.C.v. The Skeletal Muscle Anabolic Response to Plant- versus Animal-Based Protein Consumption. J. Nutr. 2015, 145, 1981–1991. [Google Scholar] [CrossRef] [Green Version]
- Pinckaers, P.J.M.; Trommelen, J.; Snijders, T.; Loon, L.J.C.v. The Anabolic Response to Plant-Based Protein Ingestion. Sports Med. 2021, 51, 59–74. [Google Scholar] [CrossRef]
- 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. 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] [Green Version]
- Mitchell, C.J.; Milan, A.M.; Mitchell, S.M.; Zeng, N.; Ramzan, F.; Sharma, P.; Knowles, S.O.; Roy, N.C.; Sjödin, A.; Wagner, K.H.; et al. The effects of dietary protein intake on appendicular lean mass and muscle function in elderly men: A 10-wk randomized controlled trial. Am. J. Clin. Nutr. 2017, 106, 1375–1383. [Google Scholar] [CrossRef] [Green Version]
- Deutz, N.E.; Bauer, J.M.; Barazzoni, R.; Biolo, G.; Boirie, Y.; Bosy-Westphal, A.; Cederholm, T.; Cruz-Jentoft, A.; Krznariç, Z.; Nair, K.S.; et al. Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group. Clin. Nutr. 2014, 33, 929–936. [Google Scholar] [CrossRef] [Green Version]
- 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]
- Paddon-Jones, D.; Rasmussen, B.B. Dietary protein recommendations and the prevention of sarcopenia. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12, 86–90. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jäger, R.; Kerksick, C.M.; Campbell, B.I.; Cribb, P.J.; Wells, S.D.; Skwiat, T.M.; Purpura, M.; Ziegenfuss, T.N.; Ferrando, A.A.; Arent, S.M.; et al. International Society of Sports Nutrition Position Stand: Protein and exercise. J. Int. Soc. Sports Nutr. 2017, 14, 20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, Y.; Li, Y.; Yang, X.; Hemler, E.C.; Fang, Y.; Zhao, L.; Zhang, J.; Yang, Z.; Wang, Z.; He, L.; et al. The dietary transition and its association with cardiometabolic mortality among Chinese adults, 1982–2012: A cross-sectional population-based study. Lancet Diabetes Endocrinol. 2019, 7, 540–548. [Google Scholar] [CrossRef] [PubMed]
Wave | Normal Muscle Mass | Low Muscle Mass | p Value |
---|---|---|---|
Sample size (N) b | 4350 (90.2) | 476 (9.8) | |
Age group (years) b | |||
60–69 | 2819 (91.3) | 270 (8.7) | 0.0005 |
70– | 1531 (88.1) | 206 (11.9) | |
Gender b | |||
Male | 1979 (88.5) | 258 (11.5) | 0.0003 |
Female | 2371 (91.6) | 218 (8.4) | |
Education level b | |||
Primary/illiterate | 2210 (89.3) | 265 (10.7) | 0.0404 |
Middle school and above | 2137 (91.1) | 210 (8.9) | |
Diabetes mellitus, n (%) b | |||
NGT | 2932 (67.5) | 356 (75.1) | 0.0026 |
IGR | 889 (20.5) | 79 (16.7) | |
T2DM | 521 (12.0) | 39 (8.2) | |
Residence area, n (%) b | |||
City | 1737 (91.9) | 153 (8.1) | 0.0009 |
Village | 2613 (89.0) | 323 (11.0) | |
Total energy intake, kcal/d a | 1817.0 (819.1) | 1755.1 (867.3) | 0.0245 |
Body mass index, kg/m2 a | 24.7 (4.4) | 19.8 (2.8) | <0.0001 |
Muscle mass, kg a | 18.0 (7.3) | 15.0 (4.2) | <0.0001 |
Relative skeletal muscle index, kg/m2 a | 7.2 (1.8) | 5.9 (1.1) | <0.0001 |
Total physical activity, MET-h/w a | 68.3 (105.0) | 60.7 (116.9) | 0.0350 |
Leisure sedentary time, h/w a | 16.0 (16.0) | 17.5 (16.0) | 0.0226 |
Dietary Protein Intake | Male | Female | ||||
---|---|---|---|---|---|---|
Normal Muscle Mass | Low Muscle Mass | p Value | Normal Muscle Mass | Low Muscle Mass | p Value | |
Total protein (g/d) | 63.2 (32.0) | 60.5 (34.9) | 0.0491 | 54.4 (28.4) | 52.5 (35.0) | 0.0426 |
Animal protein (g/d) | 22.0 (22.5) | 22.7 (24.9) | 0.3128 | 18.6 (18.6) | 18.3 (18.5) | 0.4481 |
Plant protein (g/d) | 31.8 (18.8) | 30.2 (17.4) | 0.0477 | 27.9 (16.9) | 26.1 (15.6) | 0.0468 |
Variables | Male | Female | ||||||
---|---|---|---|---|---|---|---|---|
Quartiles of Protein Intake | Coefficient | SE | p Value | Quartiles of Protein Intake | Coefficient | SE | p Value | |
Total protein intake (g/d) | ||||||||
Quartile 1 (lowest) | <48.0 | Ref | <41.3 | Ref | ||||
Quartile 2 | 48.0–62.8 | 0.52 | 0.25 | 0.0373 | 41.3–54.2 | 0.30 | 0.11 | 0.0059 |
Quartile 3 | 62.8–80.5 | 0.68 | 0.24 | 0.0049 | 54.2–70.0 | 0.47 | 0.11 | <0.0001 |
Quartile 4 (highest) | >80.5 | 0.96 | 0.24 | <0.0001 | >70.0 | 0.48 | 0.12 | <0.0001 |
p value for trend | <0.0001 | <0.0001 | ||||||
Animal protein (g/d) | ||||||||
Quartile 1 (lowest) | <12.3 | Ref | <10.8 | Ref | ||||
Quartile 2 | 12.3–22.1 | −0.12 | 0.23 | 0.6136 | 10.8–18.5 | −0.10 | 0.11 | 0.3476 |
Quartile 3 | 22.1–35.1 | 0.23 | 0.22 | 0.2926 | 18.5–29.3 | 0.11 | 0.11 | 0.3315 |
Quartile 4 (highest) | >35.1 | −0.13 | 0.21 | 0.5557 | >29.3 | 0.10 | 0.12 | 0.4122 |
p value for trend | 0.8362 | 0.0896 | ||||||
Vegetable protein (g/d) | ||||||||
Quartile 1 (lowest) | <23.1 | Ref | <20.1 | Ref | ||||
Quartile 2 | 23.1–31.5 | 0.35 | 0.24 | 0.0350 | 20.1–27.8 | 0.24 | 0.11 | 0.0274 |
Quartile 3 | 31.5–41.9 | 0.54 | 0.23 | 0.0199 | 27.8–36.9 | 0.31 | 0.11 | 0.0068 |
Quartile 4 (highest) | >41.9 | 0.76 | 0.22 | 0.0007 | >36.9 | 0.35 | 0.12 | 0.0029 |
p value for trend | 0.0006 | <0.0001 |
Male | Female | |||||
---|---|---|---|---|---|---|
Normal Muscle Mass | Low Muscle Mass | p Value | Normal Muscle Mass | Low Muscle Mass | p Value | |
Percentage of protein intake | ||||||
% morning | 0.25 (0.18) | 0.26 (0.19) | 0.6533 | 0.25 (0.18) | 0.25 (0.18) | 0.4728 |
% noon | 0.36 (0.18) | 0.37 (0.20) | 0.7106 | 0.37 (0.18) | 0.36 (0.22) | 0.5039 |
% evening | 0.36 (0.18) | 0.37 (0.19) | 0.3291 | 0.35 (0.18) | 0.37 (0.15) | 0.1439 |
Dietary protein intake | ||||||
Morning (g/meal) | 13.4 (9.7) | 13.0 (8.9) | 0.0986 | 11.9 (8.6) | 11.2 (8.2) | 0.4164 |
Noon (g/meal) | 19.7 (15.8) | 19.4 (20.9) | 0.3401 | 17.6 (14.2) | 17.0 (16.9) | 0.3978 |
Evening (g/meal) | 19.4 (15.9) | 19.9 (17.9) | 0.6941 | 16.8 (14.6) | 16.3 (12.9) | 0.9234 |
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
Ouyang, Y.; Huang, F.; Zhang, X.; Li, L.; Zhang, B.; Wang, Z.; Wang, H. Association of Dietary Protein Intake with Muscle Mass in Elderly Chinese: A Cross-Sectional Study. Nutrients 2022, 14, 5130. https://doi.org/10.3390/nu14235130
Ouyang Y, Huang F, Zhang X, Li L, Zhang B, Wang Z, Wang H. Association of Dietary Protein Intake with Muscle Mass in Elderly Chinese: A Cross-Sectional Study. Nutrients. 2022; 14(23):5130. https://doi.org/10.3390/nu14235130
Chicago/Turabian StyleOuyang, Yifei, Feifei Huang, Xiaofan Zhang, Li Li, Bing Zhang, Zhihong Wang, and Huijun Wang. 2022. "Association of Dietary Protein Intake with Muscle Mass in Elderly Chinese: A Cross-Sectional Study" Nutrients 14, no. 23: 5130. https://doi.org/10.3390/nu14235130
APA StyleOuyang, Y., Huang, F., Zhang, X., Li, L., Zhang, B., Wang, Z., & Wang, H. (2022). Association of Dietary Protein Intake with Muscle Mass in Elderly Chinese: A Cross-Sectional Study. Nutrients, 14(23), 5130. https://doi.org/10.3390/nu14235130