Document Type : Research Article (s)

Authors

1 Humanitec Junior College, Japan

2 Aichi University of Education, Japan

Abstract

Background: Quantitative analysis of echo intensity (EI) is a reliable method for discriminating between normal and neuromuscular disease-affected muscles in children. However, the effects of increased skeletal muscle fat mass and total body fat mass in healthy preschool children are yet to be determined. The purpose of this study was to compare the EI of skeletal muscles and local fat accumulation in healthy preschool children by gender and body shape using ultrasonography.
Methods: Three- to six-year-old children (149 boys and 124 girls) without any known neuromuscular disorder were included in this cross-sectional research, during the period of 2015 to 2018 in Miyazaki prefecture, Japan. Anthropometry, body composition, and EI of the biceps brachii muscle (BB) and quadriceps femoris (RF) muscle were measured by ultrasonography. Differences in anthropometric measurements and body composition divided by two types of criteria using age and sex-specific percentiles were analyzed using two-way ANOVA (P<0.05).
Results: EI at the BB of overweight children (above 90th percentile) was 9.82±3.76 for boys and 10.87±3.69 for girls. EI at the BB of normal children (10th-90th percentile) was 6.02±2.62 for boys and 6.53±2.92 for girls. EI at the BB of thin children (below 10th percentile) was 5.61±2.17 for boys and 6.52±3.49 for girls. EI at the BB of overweight children is higher than normal and thin children (P<0.001). EI at the RF of overweight children (above 90th percentile) was 16.97±5.12 for boys and 18.84±3.41 for girls. EI at the RF of normal children (10th-90th percentile) was 15.32±4.55 for boys and 16.20±3.98 for girls. EI at the RF of thin children (below 10th percentile) was 14.94±3.90 for boys and 14.58±4.94 for girls. EI at the RF of overweight children is higher than normal and thin children (P=0.024). These results were also similar for the groups created using the 25th and 75th percentiles, with the above 75th percentile group showing clearly higher values of EI.
Conclusions: Our results suggested that the accumulation of adipose tissue within skeletal muscle varies with the degree of obesity. It seems reasonable to conclude that an extreme increase in body fat might be linked to higher visceral and skeletal muscle fat (ectopic fat content).

Highlights

How to Cite: Oya C, Muramatsu E, Teramoto K. Quantitative Evaluation of Skeletal Muscle Fat Content by Measuring Echo Intensity Using Ultrasonography in Preschool Children. Int. J. School. Health. 2023;10(3):109-118. doi: 10.30476/INTJSH.2023.98323.1298.

Keywords

1) Simmonds M, Llewellyn A, Owen CG, Woolacott N. Predicting adult obesity from childhood obesity: a systematic review and meta-analysis. Obes Rev. 2016;17(2):95-107. doi: 10.1111/obr.12334. PubMed PMID: 26696565. ## 2) Guo S, Chumlea WC Roche AF, Gardner JD, Siervogel RM. The predictive value of childhood body mass index values for overweight at 35y. Am J Clin Nurt. 1994;59(4):810-9. doi: 10.1093/ajcn/59.4.810. PubMed PMID: 8147324. ## 3) Inokuchi M, Matsuo N, Takayama JI, Hasegawa T. Official Japanese reports significantly underestimate prevalence of overweight in school children: Inappropriate definition of standard weight and calculation of excess weight. Ann Hum Biol. 2009;36(2):139-45. doi: 10.1080/03014460802635213. PubMed PMID: 19194805. ## 4) Rosiek A, Frąckowiak Maciejewska N, Leksowski K, Rosiek-Kryszewska A, Leksowski Ł. Effect of Television on Obesity and Excess of Weight and Consequences of Health. Int J Environ Res Public Health. 2015;12(8):9408-26. doi: 10.3390/ijerph120809408. PubMed PMID: 26274965; PubMed Central PMCID: PMC4555288. ## 5) Singh AS, Mulder C, Twisk JWR, van Mechelen W, Chinapaw MJM. Tracking of childhood overweight into adulthood: a systematic review of the literature. Obes Rev. 2008;9(5):474-88. doi: 10.1111/j.1467-789X.2008.00475.x. PubMed PMID: 18331423. ## 6) National Task Force on Childhood Obesity, National Center for Women's and Children's Health, Ding ZY. National epidemiological survey on childhood obesity, 2006. Zhonghua Er Ke Za Zhi. 2008;46(3):179–84. PubMed PMID: 19099704. Chinese. ## 7) Must A, Jacques P, Dallal G, Bajema C, Dietz W. Long-term morbidity and mortality of overweight adolescents-a follow-up the Harvard Growth Study of 1922 to 1935. New Engl J Med. 1992;327(19):1350-5. doi: 10.1056/NEJM199211053271904. PubMed PMID: 1406836. ## 8) Teramoto K, Ishikawa T, Yamashita R, Oya C, Muramatsu E, Iezaki K, et al. Assessment of Abdominal Fat Accumulation in Preschooler Using Ultrasonography. J Human and Living Environment. 2015;22(2):33-42. doi: 10.24538/jhesj.22.2_103. Japanese. ## 9) Stock MS, Thompson BJ. Echo intensity as an indicator of skeletal muscle quality: applications, methodology, and future directions. Eur J Appl Physiol. 2021;121(2):369-380. doi: 10.1007/s00421-020-04556-6. PubMed PMID: 33221942. ## 10) Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE. Skeltal muscle sonography: a correlative study of echogenicity and morphology. J Ultrasound Med. 1993;12(2):73-7. doi: 10.7863/jum.1993.12.2.73. PubMed PMID: 8468739. ## 11) Scholten RR, Pillen S, Verrips A, Zwarts MJ. Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nurve. 2003;27(6):693-8. doi: 10.1002/mus.10384. PubMed PMID: 12766980. ## 12) Pillen S, Scholten RR, Zwarts MJ, Verrips A. Quantitative skeletal Muscle ultrasonography in children with suspected neuromuscular disease. Muscle Nurve. 2003;27(6):699-705. doi: 10.1002/mus.10385. PubMed PMID: 12766981. ## 13) Teramoto K, Iezaki K, Suda K, Oya C, Muramatsu E, Sugiyama S. Effects of habitual exercise to skeletal muscle fat content in young adult. Bulletin of Aichi University of Education, Art, Health,and Physical Education, Home Economics, Technology and Creative Arts. 2016;65:39-44. Japanese. ## 14) Teramoto K, Suda K, Kataoka Y, Oya C, Muramatsu E, Iezaki K. Effects of Short-term Moderate Training on Visceral Fat Accumulation and Skeletal Muscle Fat Content. J Human and Living Enviirronmeent. 2021;28:21-28. Japanese. ## 15) Farr JN, Loan MDV, Lohman TG, Going SB. Lower physical activity is associated with skeletal muscle fat content in girls. Med Sci Sports Exerc. 2012;44(7):1375-81. doi: 10.1249/MSS.0b013e31824749b2. PubMed PMID: 22217562; PubMed Central PMCID: PMC3819115. ## 16) Junior CASA, Martins PC, Aznar LAM, Silva DAS. Reference growth curves to identify weight status (underweight, overweight or obesity) in children and adolescents: systematic review. Br J Nutr. 2023;25:1-13. doi: 10.1017/S0007114522003786. PubMed PMID: 36695353. ## 17) Komiya S, Eto C, Otoki K, Teramoto K, Shimizu F, Shimamoto H. Gender differences in body fat of low- and high-body-mass children: relationship with body mass index. Eur J Appl Physiol. 2000;82(1-2):16-23. doi: 10.1007/s004210050646. PubMed PMID: 10879438. ## 18) Masuda T, Komiya S. A prediction equation for total body water from bioelectrical impedance in Japanese children. J Physiol Anthropol Appl Human Sci. 2004;23(2):35–9. doi: 10.2114/jpa.23.35. PubMed PMID: 15067189. ## 19) Fommon SJ, Haschke F, Ziegler EE, Nelson SE. Body composition of reference children from birth to age 10 years. Am J Clin Nutr. 1982;35:1169-75. doi: 10.1093/ajcn/35.5.1169. PubMed PMID: 7081099. ## 20) Suzuki R, Watanabe S, Hirai Y, Akiyama K, Nishide T, Matsushima Y, et al. Abdominal wall fat index, estimated by ultrasonography, for assessment of the ratio of visceral fat to subcutaneous fat in the abdomen. Am J Med. 1993;95(3):309-14. doi: 10.1016/0002-9343(93)90284-v. PubMed PMID: 8368228. ## 21) STROBE Statement-Checklist of items that should be included in reports of cross-sectional studies. STROBE Checklist. Available from: https://www.strobe-statement.org/checklists. ## 22) Gilsanz V, Kremer A, Mo AO, Wren TA, Kremer R. Vitamin D status and its relation to muscle mass and muscle fat in young women. J Clin Endocrinol Metab. 2010;95(4):1595-601. doi: 10.1210/jc.2009-2309. PubMed PMID: 20164290; PubMed Central PMCID: PMC2853984. ## 23) Manini TM, Clark BC, Nalls MA, Goodpaster BH, Ploutz-Snyder LL, Harris TB. Reduced physical activity increases intermuscular adipose tissue in healthy young adults. Am J Clin Nutr. 2007;85(2):377-84. doi: 10.1093/ajcn/85.2.377. PubMed PMID: 17284732. ## 24) Blaak EE, van Aggle-Leijssen DP, Wagenmakers AJ, Saris WH, van Baak MA. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes. 2000;49(12):2102-7. doi: 10.2337/diabetes.49.12.2102. PubMed PMID: 11118013. ## 25) Farr JN, van Loan MD, Lohman TG, Going SB. Lower physical activity is associated with skeletal muscle fat content in girls. Med Sci Sports Exerc. 2012;44(7):1375-81. doi: 10.1249/MSS.0b013e31824749b2. PubMed PMID: 22217562; PubMed Central PMCID: PMC3819115. ## 26) Johnson DL, Miller F, Subramanian P, Modlesky CM. Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr. 2009;154(5):715-20. doi: 10.1016/j.jpeds.2008.10.046. PubMed PMID: 19111321; PubMed Central PMCID: PMC2963648. ## 27) Leroy-Willig A, Willig TN, Henry-Feugeas MC, Frouin V, Marinier E, Boulier A, et al. Body composition determined with MR in patients with Duchenne muscular dystrophy, spinal muscular atrophy, and normal subjects. Magn Reson Imaging. 1997;15(7):737-44. doi: 10.1016/s0730-725x(97)00046-5. PubMed PMID: 9309604. ## 28) Zhang G, Wu L, Zhou L, Lu W, Mao C. Television watching and risk of childhood obesity: a meta-analysis. Eur J Public Health. 2015;26(1):13-8. doi: 10.1093/eurpub/ckv213. PubMed PMID: 26604324. ## 29) Prior SJ, Joseph LJ, Brandauer J, Katzel LI, Hagberg JM, Ryan AS. Reduction in midthigh low density muscle with aerobic exercise training and weight loss impacts glucose tolerance in order men. J Clin Endocrinol Metab. 2007;92(3):880-6. doi: 10.1210/jc.2006-2113. PubMed PMID: 17200170. ## 31) Sugihara T, Kondo, M, Mori, S, Yoshida I. Chronological change in preschool children's motor ability development in Japan from the 1960s to the 2000s. International Journal of Sports and Health Science, 2006;4:49-56. doi: 10.5432/ijshs.4.49. ## 31) Rech A, Radaelli R, Goltz FR, Rosa LHT, Schneider CD, Rinto RS. Echo intensity in negatively associated with functional capacity in older women. Age. 2014;36(5):9708. doi: 10.1007/s11357-014-9708-2. PubMed PMID: 25167965; PubMed Central PMCID: PMC4453939. ## 32) Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, et al. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-age and elderly persons. Eur J Appl Physiol. 2012;112(4):1519-25. doi: 10.1007/s00421-011-2099-5. PubMed PMID: 21847576. ## 33) Pillen S, Tak RO, Zwarts MJ, Lammens MMY, Verrijp KN, Arts IMP, et al. Skeletal muscle ultrasound:correlation between fibrous tissue echo intensity. Ultra Med Biol. 2009;35(3):443-6. doi: 10.1016/j.ultrasmedbio.2008.09.016. PubMed PMID: 19081667. ## 34) Heckmatt JZ, Dubowitz V. Diagnostic advantage of needle muscle biopsy and ultrasound imaging in the detection of focal pathology in a girl with limb girdle dystrophy. Muscle Nerve. 1985;8(8):705-9. doi: 10.1002/mus.880080813. PubMed PMID: 3903492. ##