Hostname: page-component-5d59c44645-dknvm Total loading time: 0 Render date: 2024-02-23T13:28:42.154Z Has data issue: false hasContentIssue false

Associations of plasma retinol and α-tocopherol levels with skeletal muscle health in Chinese children

Published online by Cambridge University Press:  21 June 2023

Jiapeng Huang
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Xuanrui Zhang
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Zhen Hong
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Xiaoping Lin
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Fengyan Chen
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Jing Lan
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Zheqing Zhang*
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
Hong Deng*
Affiliation:
Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou 510400, People’s Republic of China
*
*Corresponding authors: Zheqing Zhang, email zzqaa501@smu.edu.cn; Hong Deng, email hongd@smu.edu.cn
*Corresponding authors: Zheqing Zhang, email zzqaa501@smu.edu.cn; Hong Deng, email hongd@smu.edu.cn

Abstract

Childhood is a critical period for muscle accumulation. Studies in elders have reported that antioxidant vitamins could improve muscle health. However, limited studies have assessed such associations in children. This study included 243 boys and 183 girls. A seventy-nine-item FFQ was used to investigate dietary nutrients intake. Plasma levels of retinol and α-tocopherol were measured using high-performance liquid chromatography with MS. Dual X-ray absorptiometry was used to assess appendicular skeletal muscle mass (ASM) and total body fat. The ASM index (ASMI) and ASMI Z-score were then calculated. Hand grip strength was measured using a Jamar® Plus+ Hand Dynamometer. Fully adjusted multiple linear regression models showed that for each unit increase in plasma retinol content, ASM, ASMI, left HGS and ASMI Z-score increased by 2·43 × 10−3 kg, 1·33 × 10−3 kg/m2, 3·72 × 10−3 kg and 2·45 × 10−3 in girls, respectively (P < 0·001–0·050). ANCOVA revealed a dose–response relationship between tertiles of plasma retinol level and muscle indicators (Ptrend: 0·001–0·007). The percentage differences between the top and bottom tertiles were 8·38 %, 6·26 %, 13·2 %, 12·1 % and 116 % for ASM, ASMI, left HGS, right HGS and ASMI Z-score in girls, respectively (Pdiff: 0·005–0·020). No such associations were observed in boys. Plasma α-tocopherol levels were not correlated with muscle indicators in either sex. In conclusion, high circulating retinol levels are positively associated with muscle mass and strength in school-age girls.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

#

Co-first authors.

References

Biolo, G, Cederholm, T & Muscaritoli, M (2014) Muscle contractile and metabolic dysfunction is a common feature of sarcopenia of aging and chronic diseases: from sarcopenic obesity to cachexia - ScienceDirect. Clin Nutr 33, 737748.CrossRefGoogle Scholar
Wolfe, RR (2006) The underappreciated role of muscle in health and disease. Am J Clin Nutr 84, 475482.10.1093/ajcn/84.3.475CrossRefGoogle ScholarPubMed
Chen, F, Li, Q, Chen, Y, et al. (2022) Association of the gut microbiota and fecal short-chain fatty acids with skeletal muscle mass and strength in children. FASEB J 36, e22109.Google ScholarPubMed
Wilkinson, DJ, Piasecki, M & Atherton, PJ (2018) The age-related loss of skeletal muscle mass and function: measurement and physiology of muscle fibre atrophy and muscle fibre loss in humans. Ageing Res Rev 47, 123132.CrossRefGoogle ScholarPubMed
Carbone, JW, Mcclung, JP & Pasiakos, SM (2012) Skeletal muscle responses to negative energy balance: effects of dietary protein. Adv Nutr 3, 119126.CrossRefGoogle ScholarPubMed
Koletzko, B, Demmelmair, H, Grote, V, et al. (2016) High protein intake in young children and increased weight gain and obesity risk. Am J Clin Nutr 103, 303.10.3945/ajcn.115.128009CrossRefGoogle ScholarPubMed
Landi, F, Marzetti, E, Martone, AM, et al. (2014) Exercise as a remedy for sarcopenia. Curr Opin Clin Nutr Metab Care 17, 2531.Google ScholarPubMed
Gielen, E, Beckwée, D, Delaere, A, et al. (2021) Nutritional interventions to improve muscle mass, muscle strength, and physical performance in older people: an umbrella review of systematic reviews and meta-analyses. Nutr Rev 79, 121147.CrossRefGoogle ScholarPubMed
Cruz-Jentoft, AJ & Sayer, AA (2019) Sarcopenia. Lancet 393, 26362646.10.1016/S0140-6736(19)31138-9CrossRefGoogle ScholarPubMed
Damiano, S, Muscariello, E, La Rosa, G, et al. (2019) Dual role of reactive oxygen species in muscle function: can antioxidant dietary supplements counteract age-related sarcopenia? Int J Mol Sci 20, 3815.10.3390/ijms20153815CrossRefGoogle ScholarPubMed
Foreman, NA, Hesse, AS & Ji, LL (2021) Redox signaling and sarcopenia: searching for the primary suspect. Int J Mol Sci 22, 9045.10.3390/ijms22169045CrossRefGoogle ScholarPubMed
Fan, Z, Yang, J-Y, Guo, Y, et al. (2022) Altered levels of circulating mitochondrial DNA in elderly people with sarcopenia: association with mitochondrial impairment. Exp Gerontol 163, 111802.10.1016/j.exger.2022.111802CrossRefGoogle ScholarPubMed
Gholizade, M, Farhadi, A, Marzban, M, et al. (2022) Association between platelet, white blood cell count, platelet to white blood cell ratio and sarcopenia in community-dwelling older adults: focus on Bushehr Elderly Health (BEH) program. BMC Geriatr 22, 300.10.1186/s12877-022-02954-3CrossRefGoogle ScholarPubMed
Schaap, LA, Pluijm, SMF, Deeg, DJH, et al. (2009) Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci 64, 11831189.CrossRefGoogle ScholarPubMed
Mukund, K & Subramaniam, S (2020) Skeletal muscle: a review of molecular structure and function, in health and disease. Wiley Interdiscip Rev Syst Biol Med 12, e1462.10.1002/wsbm.1462CrossRefGoogle ScholarPubMed
Kim, J-S, Wilson, JM & Lee, S-R (2010) Dietary implications on mechanisms of sarcopenia: roles of protein, amino acids and antioxidants. J Nutr Biochem 21, 113.CrossRefGoogle ScholarPubMed
Han, X, Zhao, R, Wang, Y, et al. (2022) Dietary vitamin A intake and circulating vitamin A concentrations and the risk of three common cancers in women: a meta-analysis. Oxid Med Cell Longev 2022, 7686405.10.1155/2022/7686405CrossRefGoogle ScholarPubMed
Meulmeester, FL, Luo, J, Martens, LG, et al. (2022) Antioxidant supplementation in oxidative stress-related diseases: what have we learned from studies on alpha-tocopherol? Antioxidants 11, 2322.10.3390/antiox11122322CrossRefGoogle ScholarPubMed
Cocate, PG, Natali, AJ, Alfenas, RCG, et al. (2015) Carotenoid consumption is related to lower lipid oxidation and DNA damage in middle-aged men. Br J Nutr 114, 257264.10.1017/S0007114515001622CrossRefGoogle ScholarPubMed
Welch, AA, Jennings, A, Kelaiditi, E, et al. (2020) Cross-sectional associations between dietary antioxidant vitamins C, E and carotenoid intakes and sarcopenic indices in women aged 18–79 years. Calcif Tissue Int 106, 331342.10.1007/s00223-019-00641-xCrossRefGoogle Scholar
Semba, RD, Blaum, C, Guralnik, JM, et al. (2003) Carotenoid and vitamin E status are associated with indicators of sarcopenia among older women living in the community. Aging Clin Exp Res 15, 482487.10.1007/BF03327377CrossRefGoogle ScholarPubMed
Michelon, E, Blaum, C, Semba, RD, et al. (2006) Vitamin and carotenoid status in older women: associations with the frailty syndrome. J Gerontol A Biol Sci Med Sci 61, 600607.CrossRefGoogle ScholarPubMed
Kochlik, B, Stuetz, W, Pérès, K, et al. (2019) Associations of fat-soluble micronutrients and redox biomarkers with frailty status in the FRAILOMIC initiative. J Cachexia Sarcopenia Muscle 10, 13391346.10.1002/jcsm.12479CrossRefGoogle ScholarPubMed
Alipanah, N, Varadhan, R, Sun, K, et al. (2009) Low serum carotenoids are associated with a decline in walking speed in older women. J Nutr Health Aging 13, 170175.10.1007/s12603-009-0053-6CrossRefGoogle ScholarPubMed
Lauretani, F, Semba, RD, Bandinelli, S, et al. (2008) Low plasma carotenoids and skeletal muscle strength decline over 6 years. J Gerontol A Biol Sci Med Sci 63, 376383.CrossRefGoogle ScholarPubMed
Lauretani, F, Semba, RD, Bandinelli, S, et al. (2008) Carotenoids as protection against disability in older persons. Rejuvenation Res 11, 557563.CrossRefGoogle ScholarPubMed
Bartali, B, Frongillo, EA, Guralnik, JM, et al. (2008) Serum micronutrient concentrations and decline in physical function among older persons. JAMA 299, 308315.Google ScholarPubMed
Sahni, S, Dufour, AB, Fielding, RA, et al. (2021) Total carotenoid intake is associated with reduced loss of grip strength and gait speed over time in adults: the Framingham Offspring Study. Am J Clin Nutr 113, 437445.10.1093/ajcn/nqaa288CrossRefGoogle ScholarPubMed
Liang, J, Chen, F, Fang, G, et al. (2020) Relationship between plasma copper concentration and body fat distribution in children in China: a cross-sectional study. Biol Trace Elem Res 198, 430439.CrossRefGoogle Scholar
Liu, J, Yan, Y, Xi, B, et al. (2019) Skeletal muscle reference for Chinese children and adolescents. J Cachexia Sarcopenia Muscle 10, 155164.CrossRefGoogle ScholarPubMed
Lin, X, Zhou, Y, Li, S, et al. (2022) Markers related to oxidative stress in peripheral blood in children with autism spectrum disorder. Res Autism Spectr Disord 99, 102067.10.1016/j.rasd.2022.102067CrossRefGoogle Scholar
Chen, G, Li, Y, Liang, S, et al. (2021) Associations of dietary anthocyanidins intake with body composition in Chinese children: a cross-sectional study. Food Nutr Res 65, 4428.CrossRefGoogle ScholarPubMed
Yang, Y, Wang, G, Pang, X, et al. (2019) China Food Composition Table (Standard Edition). Beijing : Peking University Medical Press.Google Scholar
Ainsworth, BE, Haskell, WL, Herrmann, SD, et al. (2011) 2011 compendium of physical activities: a second update of codes and MET values. Med Sci Sports Exerc 43, 15751581.CrossRefGoogle ScholarPubMed
Asp, ML, Richardson, JR, Collene, AL, et al. (2012) Dietary protein and beef consumption predict for markers of muscle mass and nutrition status in older adults. J Nutr Health Aging 16, 784790.CrossRefGoogle ScholarPubMed
Cesari, M, Pahor, M, Bartali, B, et al. (2004) Antioxidants and physical performance in elderly persons: the Invecchiare in Chianti (InCHIANTI) study. Am J Clin Nutr 79, 289294.10.1093/ajcn/79.2.289CrossRefGoogle ScholarPubMed
Bo, Y, Liu, C, Ji, Z, et al. (2019) 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 38, 159164.10.1016/j.clnu.2017.12.020CrossRefGoogle Scholar
Pilleron, S, Weber, D, Pérès, K, et al. (2019) Patterns of circulating fat-soluble vitamins and carotenoids and risk of frailty in four European cohorts of older adults. Eur J Nutr 58, 379389.10.1007/s00394-017-1602-0CrossRefGoogle ScholarPubMed
Teixeira, VH, Valente, HF, Casal, SI, et al. (2009) Antioxidants do not prevent postexercise peroxidation and may delay muscle recovery. Med Sci Sports Exerc 41, 17521760.10.1249/MSS.0b013e31819fe8e3CrossRefGoogle Scholar
Rowlands, DS, Pearce, E, Aboud, A, et al. (2012) Oxidative stress, inflammation, and muscle soreness in an 894-km relay trail run. Eur J Appl Physiol 112, 18391848.10.1007/s00421-011-2163-1CrossRefGoogle Scholar
Peternelj, T-T & Coombes, JS (2011) Antioxidant supplementation during exercise training: beneficial or detrimental? Sports Med 41, 10431069.CrossRefGoogle ScholarPubMed
de Dios, O, Navarro, P, Ortega-Senovilla, H, et al. (2018) Plasma retinol levels and high-sensitivity C-reactive protein in prepubertal children. Nutrients 10, 1257.10.3390/nu10091257CrossRefGoogle ScholarPubMed
Teske, M, Melges, APB, de Souza, FIS, et al. (2014) Plasma concentrations of retinol in obese children and adolescents: relationship to metabolic syndrome components. Rev Paul Pediatr 32, 5054.10.1590/S0103-05822014000100009CrossRefGoogle ScholarPubMed
Schweigert, FJ, Klingner, J, Hurtienne, A, et al. (2003) Vitamin A, carotenoid and vitamin E plasma concentrations in children from Laos in relation to sex and growth failure. Nutr J 2, 17.10.1186/1475-2891-2-17CrossRefGoogle ScholarPubMed
Xiang, J, Nagaya, T, Huang, X-E, et al. (2008) Sex and seasonal variations of plasma retinol, α -tocopherol, and carotenoid concentrations in Japanese dietitians. Asian Pac J Cancer Prev 9, 413416.Google ScholarPubMed
Borel, P, Moussa, M, Reboul, E, et al. (2007) Human plasma levels of vitamin E and carotenoids are associated with genetic polymorphisms in genes involved in lipid metabolism. J Nutr 137, 26532659.CrossRefGoogle ScholarPubMed
Chen, M, Wang, Y, Deng, S, et al. (2022) Skeletal muscle oxidative stress and inflammation in aging: focus on antioxidant and anti-inflammatory therapy. Front Cell Dev Biol 10, 964130.CrossRefGoogle ScholarPubMed
Liao, S, Omage, SO, Bormel, L, et al. (2022) Vitamin E and metabolic health: relevance of interactions with other micronutrients. Antioxidants 11, 1785.10.3390/antiox11091785CrossRefGoogle ScholarPubMed
Palace, VP, Khaper, N, Qin, Q, et al. (1999) Antioxidant potentials of vitamin A and carotenoids and their relevance to heart disease. Free Radic Biol Med 26, 746761.CrossRefGoogle ScholarPubMed
Blaner, WS, Shmarakov, IO & Traber, MG (2021) Vitamin A and vitamin E: will the real antioxidant please stand up? Annu Rev Nutr 41, 105131.10.1146/annurev-nutr-082018-124228CrossRefGoogle ScholarPubMed
Carazo, A, Macakova, K, Matousova, K, et al. (2021) Vitamin A update: forms, sources, kinetics, detection, function, deficiency, therapeutic use and toxicity. Nutrients 13, 1703.CrossRefGoogle ScholarPubMed
Brenner, S, Brookes, MCH & Roberts, LJ (1942) The relation of liver stores to the occurrence of early signs of vitamin A deficiency in the white rat: one figure. J Nutr 23, 459471.CrossRefGoogle Scholar
Klein-Szanto, AJ, Clark, JN & Martin, DH (1980) Sexual differences in the distribution of epithelial alterations in vitamin A-deficient rats. Int J Vitam Nutr Res 50, 6169.Google ScholarPubMed
McLaren, DS (1959) Influence of protein deficiency and sex on the development of ocular lesions and survival time of the vitamin A deficient rat. Br J Ophthalmol 43, 234241.CrossRefGoogle ScholarPubMed
Rousseau, C, Nichol, JN, Pettersson, F, et al. (2004) ERbeta sensitizes breast cancer cells to retinoic acid: evidence of transcriptional crosstalk. Mol Cancer Res 2, 523531.10.1158/1541-7786.523.2.9CrossRefGoogle ScholarPubMed
Huang, HFS, Li, M-T, Von Hagen, S, et al. (1997) Androgen modulation of the messenger ribonucleic acid of retinoic acid receptors in the prostate, seminal vesicles, and kidney in the rat. Endocrinology 138, 553559.CrossRefGoogle ScholarPubMed
Courant, F, Aksglaede, L, Antignac, J-P, et al. (2010) Assessment of circulating sex steroid levels in prepubertal and pubertal boys and girls by a novel ultrasensitive gas chromatography-tandem mass spectrometry method. J Clin Endocrinol Metab 95, 8292.CrossRefGoogle ScholarPubMed
Comstock, GW, Alberg, AJ & Helzlsouer, KJ (1993) Reported effects of long-term freezer storage on concentrations of retinol, beta-carotene, and α-tocopherol in serum or plasma summarized. Clin Chem 39, 10751078.CrossRefGoogle ScholarPubMed