Next Article in Journal
Advancing the Assessment and Treatment of Comorbid Pediatric Chronic Functional Abdominal Pain (CFAP) and Restrictive Eating Disorders
Previous Article in Journal
Motor Competence between Children with and without Additional Learning Needs: A Cross-Sectional Population-Level Study
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Associations of Morphological Changes in Skeletal Muscles of Preschool Children in China Following Physical Activity

1
Graduate School of Health and Sports Science, Juntendo University, Chiba 270-1695, Japan
2
Institute of Health and Sports Science & Medicine, Juntendo University, Chiba 270-1695, Japan
3
School of Sport and Health Science, Tokai Gakuen University, Miyoshi 470-0207, Japan
4
Department of Human Structure & Function, Tokai University School of Medicine, Isehara 259-1193, Japan
5
School of Public Health, Fudan University, Shanghai 200433, China
6
School of Kinesiology, Shanghai University of Sport, Shanghai 200438, China
*
Author to whom correspondence should be addressed.
Children 2023, 10(9), 1538; https://doi.org/10.3390/children10091538
Submission received: 7 August 2023 / Revised: 26 August 2023 / Accepted: 6 September 2023 / Published: 11 September 2023

Abstract

:
Purpose: Physical activity (PA) is likely to be the most important modifiable factor in skeletal muscle development. However, the influence of PA on the skeletal muscle of preschool children has not been thoroughly investigated. The main objective of this study was to quantitatively measure PA, and then, to assess whether associations exist between site-specific muscle changes and PA in relation to sex and weight statuses in preschool children aged 3 to 4 years. Methods: A total of 86 healthy preschool children, aged 3–4 years, were instructed to wear an accelerometer for seven consecutive days. The number of steps taken daily, and minutes spent in moderate–vigorous PA (MVPA) and total PA (TPA) were recorded. Muscle thickness was measured by B-mode ultrasonography using a 5–18 MHz scanning head. Muscle thickness was measured at seven sites: the lateral forearm, upper arm, abdomen, anterior and posterior thigh, and anterior and posterior lower leg. Results: There was no significant difference between boys and girls in terms of MVPA and TPA on weekdays and weekends. According to the linear regression models, after adjusting for daylight duration, the muscle of the posterior thigh was significantly positively associated (p < 0.05) with daily steps and MVPA on weekdays for boys and girls, respectively. Conclusions: We found that the muscle thickness of the posterior thigh in preschool children was significantly positively associated with PA, as measured by daily steps and MVPA. We suggest that for the overall health and well-being of preschool children, the levels of PA should be maintained and/or increased, and preferably transformed into a regular part of daily living.

1. Background

Childhood is a key period for skeletal growth, whereby the body increases in size, yet, notably, the changes in the proportions of muscle and fat mass are influenced by gender. Previous studies have reported differences in skeletal muscle and fat mass in children [1] and gender-based disparities have also been documented [2,3]. However, evaluation of the results of muscle thickness in the forearm, thigh, and lower leg showed no significant differences by sex in children and adolescents aged 0–18 years [4]. It is difficult to measure skeletal muscle thickness in children and adolescents, partly because the site of the examinable skeletal muscle can only be located in the upper or lower limbs.
Skeletal muscle is highly plastic and is capable of responding to a variety of stimuli [5,6]. Over the past few decades, the quadriceps muscle group has frequently served as an indicator of age-related alterations in muscle and lower limb strength [7]. Several studies have reported that daily PA provides an important stimulus to the musculoskeletal system, which can improve muscle development. Some studies have suggested that children and adolescents with higher fat masses have lower-than-expected daily PA and are at an increased risk of fractures [8,9]. Growing evidence suggests that daily PA in children and adolescents is negatively associated with total body fat [10,11]. Therefore, additional studies are needed to better understand the association between daily PA levels and body fat percentages, which will provide useful insights for interventional studies that focus on enhancing daily PA and reducing the body fat percentages in the target group.
Recent research showed that reduced PA levels are a strong predictor of weight gain and/or obesity in children and are associated with the risk of cardiovascular disease factors [12,13]. In addition, the role of muscle thickness has been increasingly recognized in the prevention of chronic disease in adults [14], and the features of metabolic syndrome have been negatively associated with body fat percentages in men [15] and women [16]. Obesity is associated with an increase in muscle mass [17], suggesting that the strength production capacity of obese individuals is higher than that of non-obese participants. However, because obesity is also associated with a decrease in muscle quality [18,19] and a higher body fat percentage owing to less physical activity [20], the muscle gain yielded may eventually be of too poor quality to offset the increase in body fat percentage associated with reduced PA [21]. It is important to understand whether the relationship between PA and muscle thickness identified in children is independently related to weight status in children, in order for effective evidence-based prevention and treatment strategies to be implemented as early as possible.
We previously reported that the quantity and intensity of PA is predominantly related to weight status in children [22], yet it is unclear whether preschool children are also associated with PA and skeletal muscle. Therefore, further studies would be beneficial to determine whether daily PA and/or muscle thickness could be proposed as health markers at these ages. In view of the above, the main objectives of this study were to:
(1)
Evaluate the skeletal muscle thickness and objectively measure PA;
(2)
Assess whether associations exist between site-specific muscle thickness and level of PA with regard to sex and weight status in preschool children aged 3 to 4 years.

2. Methods

2.1. Participants

A total of 113 healthy preschool children, aged 3–5 years were selected, using the selection criteria for admission into the study: attendance at a preschool, permission from parents to participate in this study, and no injuries or current illnesses reported. The parents of each subject provided informed consent in line with research protocols adhering to the Declaration of Helsinki, which was approved by the ethics committee of Juntendo University.

2.2. Anthropometrics Data

In 2017, all anthropometric data were collected by trained staff under the supervision of a school nurse. Height and body weight were measured using a portable stadiometer and portable digital scale (TCS-200-RT; Yao Yi, Shanghai, China), respectively. Weight status (i.e., underweight, normal weight, and overweight/obese) was determined according to the age- and sex-specific cutoffs of the Working Group on Obesity in China (WGOC) [23]. Table A1 describes BMI standard cutoff criteria for the overweight and obese classification of preschool children in China.

2.3. Muscle Thickness

Muscle thickness and fat thickness (FTs) were measured via B-mode ultrasonography using a 5–18 MHz scanning head (Noblus; Hitachi, Tokyo, Japan). The scanning head was prepared using a water-soluble transmission gel that provided acoustic contact without depressing the skin surface. MTs and FTs were obtained at seven sites on the anterior and posterior surfaces of the body [24]. The seven anatomical landmarks for the chosen sites were defined as follows: the upper arm (UA) site was approximately 60% distal to the entire upper arm between the lateral epicondyle of the humerus near the elbow and the acromial process of the scapula at the shoulder; the forearm (FA) site was on the anterior surface, 30% proximal to Y between the styloid process of the wrist and the head of the radius at the elbow; the abdominal (AB) site was at a distance of 3 cm to the right of the umbilicus; the anterior thigh (AT) and posterior thigh (PT) sites were on the anterior and posterior surfaces of the upper leg, midway between the lateral condyle of the femur at the knee and the greater trochanter at the hip; lastly, anterior (AL) and posterior (PL) lower leg sites were approximately 30% proximal to the talus between the lateral malleolus of the fibula at the ankle and the lateral condyle of the tibia at the knee.

2.4. Physical Activity

We measured PA using a uniaxial Kenz GS AC (Lifecorder, Suzuken Co., Ltd., Nagoya, Japan; 60 g). Each child attached the accelerometer (AC) to their waist and wore it from the time they got up in the morning until they went to bed. They were instructed to wear the AC from Monday to Sunday, providing seven consecutive days of data. The accelerometer has been previously validated in the study of children and adolescents [25,26,27]. According to the scale, distinctions were made regarding intensity (levels 1–3, 4–6, and 7–9), where light PA (LPA) was defined as AC intensity levels of 1–3 and 1.5–2.9 metabolic equivalent of task; moderate PA (MPA): AC intensity levels of 4–6 and 3.0–5.9 METs; vigorous PA (VPA): AC intensity levels of 7–9 and ≥6.0 METs [28,29]. We recorded crude step counts to estimate activity levels, and the time spent in MVPA (≥3.0 METs) was calculated as the sum of the MPA and VPA minutes, and TPA = LPA + MPA + VPA for each day. The study required at least four days of recording (including weekends), with a minimum of 10 h of wear time per day for inclusion in the subsequent analysis [30]. We excluded days when no signal was detected by the AC for more than one hour, with this period regarded as non-wearing time.

2.5. Data Analysis

The results are presented as mean and standard deviation (SD). We conducted a two-way analysis of variance (ANOVA) to determine the variability in each muscle thickness and daily PA outcome (steps, MVPA, and TPA) among the sexes, and weight status. A 2 (sex: boys and girls) × 2 (weight status: normal and overweight/obese) ANOVA was used to assess variability during weekdays and weekends. ANOVA with Bonferroni post hoc test was used to determine their significance.
To determine the bivariate relationships between all indicators of muscle thickness and daily PA, we conducted linear regression models (reported as Pearson’s correlation coefficients) by inserting all indicators of muscle thickness as independent variables and daily PA as dependent variables. Two models were used in this study. Model 1 was an unadjusted analysis of the muscle thickness, fat, and PA. Model 2 was adjusted for height, weight, and duration of daylight. There was no interaction noted between monthly age groups and the PA outcomes, which indicates that the pattern of the association with muscle thickness and daily PA was similar in 3- and 4-year-old preschool children. Therefore, the analysis grouped children aged three and four years together and included the monthly age as a covariate in the model.
Statistical analysis was conducted using SPSS software (version 22.0; SPSS Inc., IBM, NY, USA: IBM Corp.), and the level of significance was set at p < 0.05.
The study report followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement (Table S1).

3. Results

3.1. Participant Characteristics

A total of 86 preschool children (47 boys and 39 girls) met the inclusion criteria and were included in the analyses (Table 1). For preschool children, the median age was 49 ± 6 months for boys and girls, as shown in Table 2. Boys and girls had similar physical characteristics. Of the study population, 13.8% of the boys and 8.6% of the girls were classified as overweight or obese according to the WGOC thresholds of BMI. Boys and girls in the weight status groups had significantly higher weights and BMI than those in the NW group (Table A1, p < 0.05). The sample selection process is detailed in Figure 1.

3.2. Muscle Thickness and Fat Thickness Values

Descriptive characteristics and ultrasound MT measurements of preschool children in relation to sex and weight status are reported in Figure 2. Girls had significantly lower muscle thicknesses in the UA, FA, and AL than boys. For boys, the OW/OB group had significantly greater thickness in the UA, FA, AT, PT, AL, and PL than those in the NW group (p < 0.05). For girls, the OW/OB group had significantly greater FA, AT, PT, AL, and PL thickness.
All indicators of fat thickness values were significantly higher in girls than in boys as well as in the OW/OB group compared to their NW peers (p < 0.05).

3.3. Daily Physical Activity Outcomes

The daily physical activity outcomes for the boys and girls are shown in Table 2. There was no significant difference in steps, MVPA, and TPA between the boys and girls, except for in the TPA on weekends (girls were significantly less active than boys (107.8 min ± 22.4 vs. 124.0 min ± 24.4, p < 0.05)).
According to weight status, no significant differences were found in steps, MVPA, and TPA between the NW and OW/OB groups on both the weekdays and weekends in either the boys or girls (Table A2).

3.4. Association between Muscle Thickness and Fat Thickness Values in Line with Physical Activity

The results of the linear regression models are shown in Table 3. For boys, the AB muscle was positively associated with daily steps and MVPA on weekdays. The PT muscle was positively associated with steps on both weekdays and weekends and MVPA on weekends (p < 0.05). Regarding fat thickness, only FA was negatively associated with MVPA on weekdays (p < 0.05).
In girls, the PT and PL muscles were positively associated with daily steps, MVPA, and TPA on weekends. With regards to fat thickness, PT was negatively associated with daily steps and MVPA on weekdays, whereas PL was negatively associated with MVPA on weekdays (p < 0.05).
The adjusted associations between muscle thickness and fat thickness with PA for each characteristic measurement are shown in Table 4. In the adjusted analyses, the most consistent results were established for the PT muscle, which was significantly positively associated with daily steps and MVPA on weekdays and TPA on both weekdays and weekends. Moreover, the fat thickness in the UA was negatively associated with daily steps, MVPA, and TPA on weekdays in boys (p < 0.05).
For girls, in the adjusted analyses, the most consistent results were established for the PT and PL muscles, which were significantly positively associated with daily steps and MVPA on weekdays, and MVPA on weekends, respectively. Moreover, AB was positively associated with all PA outcomes on weekdays and weekends. For fat thickness, PT and PL were inversely associated with daily steps and MVPA on weekdays, independent of covariates, respectively (p < 0.05).

4. Discussion

This study examined the association between muscle thickness and PA using the weight status of Chinese preschool children after adjusting for several potential confounding factors. These findings expand on the current literature since this is, to the best of our knowledge, the first study to report an association between measures of muscle thickness and PA in preschoolers in China. Our data showed that the muscle thicknesses of preschool children had significant positive associations with PA, both in daily steps and MVPA. The relationships were stronger for the lower legs than for the arms, and for girls than for boys.
In this study, after adjusting for monthly age, height, and weight, we observed that the relationships for the muscle thickness of the lower limb were positively associated with daily steps and MVPA on weekdays for boys. Similar relationships were also observed in the AB muscle, and the lower limb was positively associated with daily steps and MVPA on both weekdays and weekends for girls. These results suggest that decreasing muscle thickness and increasing fat thickness in early childhood (OW/OB) may affect fitness performance and PA.
Our results indicated that the positive associations between muscle thickness and the objective measurements of PA, especially a moderate–vigorous intensity, correlated more strongly with lower limb muscle mass than with upper limb muscle mass. In a recent study, positive associations were noted between vigorous physical activity (PA) and the strength of the lower-body muscles in assessments conducted on both adolescents and adults [7]. Few studies have investigated the association between muscle thickness and PA according to weight status in preschool children. There is some evidence that showed a significantly positive relationship between walking speed and knee extension torque with both daily steps and intensity of activity >3 METs [31]. These observations may indicate a causal relationship, since walking, the primary component of our indices of habitual activity, is more likely to maintain muscle function in the legs than in the arm [32]. Additionally, even after accounting for various potential confounding factors, the associations we observed with objectively measured PA levels remained statistically significant. Recent meta-analyses focusing on PA and metabolic outcomes have shown that a mere 10 min increment in MVPA is linked to reduced waist circumference and lower fasting insulin levels [11,33]. To our knowledge, no previous study has reported an association between muscle thickness and PA in preschool children. Thus, in the present study, the lack of daily steps and MVPA may be major contributing factors to the increasing prevalence of overweight or obese children.
Our findings showed a significant effect of sex on all indicators of fat thickness, yet no difference in muscle thickness. Cross-sectional studies have shown consistent gender-related variations in muscle thickness among children aged 3–18 years, both in boys and girls [2], although the differences were only observed in the upper arm. In Western countries, the percentage body fat rate rapidly increases to 25% one year after birth, then, decreases around the age of 5 years. Girls begin to increase in body fat percentage around the age of 6 years, and it continues to increase until adulthood. Boys, however, only begin to increase their body fat percentage from the age of 7 years and peak at 11 years old, after which a decrease is observed due to the rapid increase in fat-free mass [3]. Therefore, our findings affirm the outcomes of previous research, underscoring that boys generally exhibit significantly lower body fat levels than girls. Conversely, this study reveals that boys tend to have notably greater muscle thickness in certain ranges compared to girls [34,35]. In our study, we did not observe significant gender disparities in BMI between boys and girls, which is consistent with findings from previous research [35]. The sex-specific pattern of fat accumulation during childhood was characterized by a steady increase in subcutaneous fat accumulation in girls. From these considerations, it was shown that sex differences do exist in the fat thickness of the upper and lower limbs from infancy to early childhood.
Our results also revealed no significant differences in PA between weekdays and weekends among NW and OW/OB children in these age groups, although the intensity level of PA was higher in the group of preschool children who were not overweight/obese. Comparable information was disclosed in a Portuguese study involving preschool children in the same age group [36]. On the contrary, numerous studies conducted in older children (aged > 6 years) have demonstrated a strong and statistically significant inverse connection between weight status and PA in overweight and obese children, who engaged in notably less PA compared to their normal weight counterparts [22,37]. Extending these findings in children, a recent study revealed a close relationship between the body fat percentage and the level of PA, whereby children with a higher percentage of body fats were less physically active, both in terms of steps per day and moderate to vigorous physical activity [20]. Moreover, a recent study has furnished evidence that a mere 10 min increase in daily moderate or vigorous physical activity (PA) can result in an average elevation of 1–2% in bone stiffness on a substantial sample of children aged 2–10 years [10]. The fact that we did not find a correlation between weight status and daily PA in preschool children leads us to conclude that, in younger children, the natural drive to be active is not influenced by a higher BMI, as it seems to be in old children. Therefore, it is essential to initiate preventive interventions in this age group. The urgent need for early intervention is underlined by the fact that PA seems to decrease from childhood to adolescence. As there are no validated obesity prevention strategies for childhood and adolescence, early identification of potential risk factors is crucial. In adults, the level of PA may predict the risk of developing chronic diseases in the future. However, our results suggest that risk prediction for obesity and associated diseases may not be assumed by PA in preschool children, but PA may be of increasing importance during the course of childhood development [38]. Thus, promotion of PA that starts as early as possible may prevent chronic diseases later in life.
According to sex and the day of the week (weekdays and weekends), this study did not identify differences in PA between sex and the day of the week. This is consistent with some [39,40], but not all previous studies [41,42]. Previous research has suggested that the differences in sex and the day of the week might be explained by the fact that PA in preschool children is not greatly influenced by the environment, but rather by personal factors [39]. Rowlands et al. [43] found that PA decreased in children aged 9 to 11 years during weekends. These findings suggest that the tendency of children to be less active during weekends begins at a very young age, which might require special attention in future activity interventions. Moreover, we also believe that issues, such as the involvement of family and the perception of an unfavorable family environment, together with social roles for girls, may play a role in why children are less active [44] over the weekend.
This study has some limitations. Since our sample only included preschool children from a large metropolitan area, it makes it difficult to generalize these findings. Accelerometers also possess certain limitations when it comes to evaluating overall activity levels. It is crucial to acknowledge that, particularly for preschool children, a shorter accelerometer interval (e.g., 5 s) is strongly advised due to the sporadic nature of their physical activity [45]. As a consequence, there is a potential for underestimating sedentary time and vigorous PA, while moderate PA may be overestimated due to the shorter accelerometer interval recommended for preschool children. This aspect should be considered when interpreting data related to physical activity levels for children from an early age. Although we controlled for several potential confounders, such as age, height, and weight, we cannot be certain that other unmeasured confounders, such as dietary intake or genetic variation, did not have an influence on our findings. Therefore, future studies should address these issues.

5. Conclusions

In conclusion, our study demonstrated that higher muscle and lower fat thickness were associated with higher levels of PA, especially MVPA. The findings also suggest that preschool children seem to be engaging adequately in PA. Developing health habits at this early stage increases the probability of these habits continuing into later life. It may be as important to maintain and/or increase the amount of PA in preschool children as it is to foster awareness of the importance of PA and transform it into a regular daily habit.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/children10091538/s1, Table S1: Checklist of items that should be included in reports of cross-sectional studies.

Author Contributions

P.D. performed the draft of the manuscript, data interpretation, and statistical analysis. H.O., T.N. and D.K. conceived of the study, participated in its design and helped to draft the manuscript. D.L., K.S. and H.N. participated in the design and revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by JSPS KAKENHI Grant Number 16H07183 and 20K19610, the Juntendo University Japanese Center for Research on Women in Sport, the Juntendo University Institute of Health and Sports Science & Medicine and the Joint Research Program of Juntendo University, Faculty of Health and Sports Science. The experiments comply with the current laws of the country in which they were performed.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Institutional Review Board of Juntendo University (HSS #28-91 and 20 September 2016).

Informed Consent Statement

Informed consent was obtained from the parents for each young child.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy restrictions.

Acknowledgments

The authors are grateful to all the children who took part in this study, their caregivers, and all the supporting staff of this study.

Conflicts of Interest

The authors have no conflict of interest to declare.

Abbreviations

PA: physical activity; total PA (TPA); MVPA: moderate–vigorous physical activity; light PA (LPA); moderate PA (MPA); vigorous PA (VPA); accelerometer (AC); BMI: body mass index; muscle thickness (MTs); fat thickness (FTs); upper arm (UA); forearm (FA) abdominal (AB); anterior thigh (AT); posterior thigh (PT); anterior lower leg (AL); posterior lower leg (PL).

Appendix A

Table A1. BMI cutoff point for preschool children in China.
Table A1. BMI cutoff point for preschool children in China.
BoysGirls
OverweightObeseOverweightObese
3.0 years old16.818.116.918.3
3.5 years old16.617.916.818.2
4.0 years old16.517.816.718.1
4.5 years old16.417.816.618.1
5.0 years old16.517.916.618.2
5.5 years old16.618.116.718.3
6.0 years old16.818.416.718.4
Note: BMI: body mass index.
Table A2. Daily physical activity outcomes of NW and OW/OB for boys and girls.
Table A2. Daily physical activity outcomes of NW and OW/OB for boys and girls.
Boys
NWOW/OBBody Shape
Difference
Daily Difference
Weekday:
Daily steps (steps/day)12,159 ± 248712,292 ± 29550.8610.406
MVPA (min/day)40.4 ± 11.137.5 ± 11.80.6380.518
TPA (min/day)123.0 ± 23.6128.0 ± 28.70.6210.649
Weekend:
Daily steps (steps/day)11,823 ± 394310,829 ± 44110.664
MVPA (min/day)40.3 ± 19.036.2 ± 14.00.750
TPA
(min/day)
117.1 ± 37.0110.9 ± 48.90.781
Girls
NWOW/OBBody Shape
Difference
Daily difference
Weekday:
Daily steps (steps/day)10,845 ± 252610,561 ± 15840.7680.552
MVPA (min/day)36.9 ± 12.434.2 ± 9.10.6250.428
TPA (min/day)108.0 ± 23.7106.9 ± 12.50.8360.697
Weekend:
Daily steps (steps/day)10281 ± 515510589 ± 14250.122
MVPA (min/day)35.2 ± 25.336.7 ± 9.00.454
TPA
(min/day)
101.8 ± 46.3100.1 ± 13.10.062
Note: mean ± SD; NW: normal weight; OW/OB: overweight/obese; MVPA: moderate–vigorous physical activity; TPA: total physical activity.

References

  1. Ellis, K.J.; Shypailo, R.J.; Abrams, S.A.; Wong, W.W. The reference child and adolescent models of body composition—A contemporary comparison. Ann. N. Y. Acad. Sci. 2000, 904, 374–382. [Google Scholar] [CrossRef] [PubMed]
  2. Ruff, C. Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 2003, 33, 317–329. [Google Scholar] [CrossRef] [PubMed]
  3. Veldhuis, J.D.; Roemmich, J.N.; Richmond, E.J.; Rogol, A.D.; Lovejoy, J.C.; Sheffield-Moore, M.; Mauras, N.; Bowers, C.Y. Endocrine control of body composition in infancy, childhood, and puberty. Endocrinol. Rev. 2005, 26, 114–146. [Google Scholar] [CrossRef] [PubMed]
  4. Baughan, B.; Brault-Dubuc, M.; Demirjian, A.; Gagnon, G. Sexual dimorphism in body composition changes during the pubertal period: As shown by French-Canadian children. Am. J. Phys. Anthropol. 1980, 52, 85–94. [Google Scholar] [CrossRef]
  5. Corbin, C.B.; Pangrazi, R.P.; Franks, B.D. Definitions: Health, Fitness, and Physical Activity. President’s Council on Physical Fitness and Sports Research Digest. 2000. Available online: http://www.fitness.gov/digest_mar2000.htm (accessed on 9 March 2000).
  6. Schaap, L.A.; Pluijm, S.M.; Deeg, D.J.; Visser, M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am. J. Med. 2006, 119, 526.e9–526.e17. [Google Scholar] [CrossRef]
  7. Abe, T.; Sakamaki, M.; Yasuda, T.; Bemben, M.G.; Kondo, M.; Kawakami, Y.; Fukunaga, T. Age-related, site-specific muscle loss in 1507 Japanese men and women aged 20 to 95 years. J. Sports Sci. Med. 2011, 10, 145–150. [Google Scholar]
  8. Skaggs, D.L.; Loro, M.L.; Pitukcheewanont, P.; Tolo, V.; Gilsanz, V. Increased body weight and decreased radial cross-sectional dimensions in girls with forearm fractures. J. Bone Miner. Res. 2001, 16, 1337–1342. [Google Scholar] [CrossRef]
  9. Goulding, A.; Grant, A.M.; Williams, S.M. Bone and body composition of children and adolescents with repeated forearm fractures. J. Bone Miner. Res. 2005, 20, 2090–2096. [Google Scholar] [CrossRef]
  10. Herrmann, D.; Buck, C.; Sioen, I.; Kouride, Y.; Marild, S.; Molnar, D.; Mouratidou, T.; Pitsiladis, Y.; Russo, P.; Veidebaum, T.; et al. Impact of physical activity, sedentary behaviour and muscle strength on bone stiffness in 2–10-year-old children-cross-sectional results from the IDEFICS study. Int. J. Behav. Nutr. Phys. Act. 2015, 12, 112. [Google Scholar] [CrossRef]
  11. Hasselstrom, H.; Hansen, S.E.; Froberg, K.; Andersen, L.B. Physical fitness and physical activity during adolescence as predictors of cardiovascular disease risk in young adulthood. Danish Youth and Sports study. An eight-year follow-up study. Int. J. Sports Med. 2002, 23, S27–S31. [Google Scholar] [CrossRef]
  12. Neef, M.; Weise, S.; Adler, M.; Sergeyev, E.; Dittrich, K.; Korner, A.; Kiess, W. Health impact in children and adolescents. Best Pract. Res. Clin. Endocrinol. Metab. 2013, 27, 229–238. [Google Scholar] [CrossRef] [PubMed]
  13. Singh, A.S.; Mulder, C.; Twisk, J.W.; van Mechelen, W.; Chinapaw, M.J. Tracking of childhood overweight into adulthood: A systematic review of the literature. Obes. Rev. 2008, 9, 474–488. [Google Scholar] [CrossRef] [PubMed]
  14. Ruiz, J.R.; Sui, X.; Lobelo, F.; Morrow, J.R.; Jackson, A.W. Association between muscular strength and mortality in men: Prospective cohort study. Br. Med. J. 2008, 337, a439. [Google Scholar] [CrossRef] [PubMed]
  15. Jurca, R.; Lamonte, M.J.; Barlow, C.E.; Kampert, J.B.; Church, T.S.; Blair, S.N. Association of muscular strength with incidence of metabolic syndrome in men. Med. Sci. Sports Eexerc 2005, 37, 1849–1855. [Google Scholar] [CrossRef]
  16. Wijndaele, K.; Duvigneaud, N.; Matton, L.; Duquet, W.; Thomis, M.; Beunen, G.; Lefevre, J.; Philippaerts, R.M. Muscular strength, aerobic fitness, and metabolic syndrome risk in Flemish adults. Med. Sci. Sports Exerc. 2007, 39, 233–240. [Google Scholar] [CrossRef]
  17. Janssen, I.; Heymsfield, S.B.; Wang, Z.M.; Ross, R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J. Appl. Physiol. 2000, 89, 81–88. [Google Scholar] [CrossRef]
  18. Koster, A.; Ding, J.Z.; Stenholm, S.; Caserotti, P.; Houston, D.K.; Nicklas, B.J.; You, T.J.; Lee, J.S.; Visser, M.; Newman, A.B.; et al. Does the Amount of Fat Mass Predict Age-Related Loss of Lean Mass, Muscle Strength, and Muscle Quality in Older Adults? J. Gerontol. Ser. A Biomed. Sci. Med. Sci. 2011, 66, 888–895. [Google Scholar] [CrossRef]
  19. Goodpaster, B.H.; Carlson, C.L.; Visser, M.; Kelley, D.E.; Scherzinger, A.; Harris, T.B.; Stamm, E.; Newman, A.B. Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study. J. Appl. Physiol. 2001, 90, 2157–2165. [Google Scholar] [CrossRef]
  20. Telford, R.D.; Cunningham, R.B.; Telford, R.M.; Riley, M.; Abhayaratna, W.P. Determinants of childhood adiposity: Evidence from the Australian LOOK study. PLoS ONE 2012, 7, e50014. [Google Scholar] [CrossRef]
  21. Jensen, G.L.; Friedmann, J.M. Obesity is associated with functional decline in community-dwelling rural older persons. J. Am. Geriatr. Soc. 2002, 50, 918–923. [Google Scholar] [CrossRef]
  22. Pengyu, D.; Noriko, I.S.; Liangfu, Z.; Hisashi, N. Changes in physical activity and weight status of Chinese children: A retrospective longitudinal study. Jpn. J. Phys. Fit. Sports Med. 2016, 5, 247–256. [Google Scholar]
  23. Li, H.; Ji, C.Y.; Song, X.N.; Zhang, Y.Q. Body mass index growth curves for Chinese children and adolescents aged 0 to 18 years. Chin. J. Pediatr. 2009, 47, 493. [Google Scholar]
  24. Hadda, V.; Khilnani, G.C.; Kumar, R.; Dhunguna, A.; Mittal, S.; Khan, M.A.; Madan, K.; Mohan, A.; Guleria, R. Intra- and Inter-observer Reliability of Quadriceps Muscle Thickness Measured with Bedside Ultrasonography by Critical Care Physicians. Indian J. Crit. Care Med. 2017, 21, 448–452. [Google Scholar] [PubMed]
  25. Sasayama, K.; Adachi, M. Association between activity level assessed by a uniaxial accelerometer and metabolic equivalents during walking and running in male youths. Jpn. J. Phys. Fit. Sports Med. 2016, 65, 265–272. [Google Scholar]
  26. Adachi, M.; Sasayama, K.; Hikihara, Y.; Okishima, K.; Mizuuchi, H.; Sunanmi, Y.; Shiomi, M.; Nishimuta, M. Assessing daily physical activity in elementary school students used by accelerometer: A validation study against doubly labeled water method. Jpn. J. Phys. Fit. Sports Med. 2007, 56, 347–355. [Google Scholar]
  27. Jimenez-Pavon, D.; Kelly, J.; Reilly, J.J. Associations between objectively measured habitual physical activity and adiposity in children and adolescents: Systematic review. Int. J. Pediatr. Obes. 2010, 5, 3–18. [Google Scholar] [CrossRef]
  28. Hikihara, Y.; Sasayama, K.; Okishima, K.; Mizuuchi, H.; Yoshitake, Y.; Adachi, M.; Takamatsu, K. The difference of relationships between physical activity variables and physical fitness in children and adolescents: With special reference to amount and intensity of physical activity. Jpn. J. Phys. Fit. Sports Med. 2007, 56, 327–339. [Google Scholar]
  29. Adachi, M.; Sasayama, K.; Ando, R.; Tanaka, Y.; Okishima, K.; Mizuuchi, H. Relationship between walking or running speed and exercise intensity measured by Accelerometer on Japanese school children and adolescens. Bull. Fac. Eudc. Okayama Univ. 2005, 128, 141–145. (In Japanese) [Google Scholar]
  30. Trost, S.G.; Loprinzi, P.D.; Moore, R.; Pfeiffer, K.A. Comparison of accelerometer cut points for predicting activity intensity in youth. Med. Sci. Sports Eexerc 2011, 43, 1360–1368. [Google Scholar] [CrossRef] [PubMed]
  31. Aoyagi, Y.; Shephard, R.J. Steps per day: The road to senior health? Sports Med. 2009, 39, 423–438. [Google Scholar] [CrossRef]
  32. Lindström, P.J.; Suni, J.H.; Nygård, C.H. Associations of leisure-time physical activity with balance and lower extremity strength: A validation of the neuromuscular part of the Physical Activity Pie. J. Phys. Act. Health 2009, 6, 493–502. [Google Scholar] [CrossRef] [PubMed]
  33. Ekelund, U.; Luan, J.; Nygard, C.H. Moderate to vigorous physical activity and sedentary time and cardiometabolic risk factors in children and adolescents. JAMA 2012, 307, 704–712. [Google Scholar] [CrossRef] [PubMed]
  34. Garnett, S.P.; Hogler, W.; Blades, B.; Baur, L.A.; Peat, J.; Lee, J.; Cowell, C.T. Relation between hormones and body composition, including bone, in prepubertal children. Am. J. Clin. Nutr. 2004, 80, 966–972. [Google Scholar] [CrossRef]
  35. Sakai, T.; Demura, S.; Fujii, K. Age-related changes of body composition structure based on differences in morphological qualities of Japanese preschool children. J. Physiol. Anthropol. 2011, 30, 213–221. [Google Scholar] [CrossRef]
  36. Vale, S.M.; Santos, R.M.; da Cruz Soares-Miranda, L.M.; Moreira, C.M.; Ruiz, J.R.; Mota, J.A. Objectively measured physical activity and body mass index in preschool children. Int. J. Pediatr. 2010, 2010, 479439. [Google Scholar] [CrossRef] [PubMed]
  37. Dorsey, K.B.; Herrin, J.; Krumholz, H.M. Patterns of moderate and vigorous physical activity in obese and overweight compared with non-overweight children. Int. J. Pediatr. Obes. 2011, 6, e547–e555. [Google Scholar] [CrossRef]
  38. Bluher, S.; Markert, J.; Herget, S.; Yates, T.; Davis, M.; Muller, G.; Waldow, T.; Schwarz, P.E. Who should we target for diabetes prevention and diabetes risk reduction? Curr. Diabetes Rev. 2012, 12, 147–156. [Google Scholar] [CrossRef]
  39. Taylor, R.W.; Murdoch, L.; Carter, P.; Gerrard, D.F.; Williams, S.M.; Taylor, B.J. Longitudinal study of physical activity and inactivity in preschoolers: The FLAME study. Med. Sci. Sports Eexerc. 2009, 41, 96–102. [Google Scholar] [CrossRef]
  40. Verbestel, V.; Van Cauwenberghe, E.; De Coen, V.; Maes, L.; De Bourdeaudhuij, I.; Cardon, G. Within- and Between-Day Variability of Objectively Measured Physical Activity in Preschoolers. Pediatr. Exerc. Sci. 2011, 23, 366–378. [Google Scholar] [CrossRef]
  41. Schmutz, E.A.; Leeger-Aschmann, C.S.; Radtke, T.; Muff, S.; Kakebeeke, T.H.; Zysset, A.E.; Messerli-Burgy, N.; Stulb, K.; Arhab, A.; Meyer, A.H.; et al. Correlates of preschool children’s objectively measured physical activity and sedentary behavior: A cross-sectional analysis of the SPLASHY study. Int. J. Behav. Nutr. Phys. Act. 2017, 14, 1. [Google Scholar] [CrossRef]
  42. Cardon, G.M.; De Bourdeaudhuij, I.M. Are preschool children active enough? Objectively measured physical activity levels. Res. Q. Exerc. Sport. 2008, 79, 326–332. [Google Scholar] [CrossRef] [PubMed]
  43. Rowlands, A.V.; Pilgrim, E.L.; Eston, R.G. Patterns of habitual activity across weekdays and weekend days in 9–11-year-old children. Prev. Med. 2008, 46, 317–324. [Google Scholar] [CrossRef] [PubMed]
  44. Dowda, M.; Pfeiffer, K.A.; Brown, W.H.; Mitchell, J.A.; Byun, W.; Pate, R.R. Parental and environmental correlates of physical activity of children attending preschool. Arch. Pediatr. Adolesc. Med. 2011, 165, 939–944. [Google Scholar] [CrossRef]
  45. Edwardson, C.L.; Gorely, T. Epoch length and its effect on physical activity intensity. Med. Sci. Sport. Eexerc 2010, 42, 928–934. [Google Scholar] [CrossRef] [PubMed]
Figure 1. STROBE study flow of participants.
Figure 1. STROBE study flow of participants.
Children 10 01538 g001
Figure 2. Muscle thickness and fat thickness outcomes of preschool children. (A) Muscle thickness of boys and girls; (B) Fat thickness of girls; (C) Muscle thickness between NW and OW/OB boys; (D) Fat thickness between NW and OW/OB boys; (E) Muscle thickness between NW and OW/OB girls; (F) Fat thickness between NW and OW/OB girls. NW: normal weight; OW/OB: overweight/obese; UA: upper arm; FA: forearm; AB: abdomen; AT: anterior thigh; PT: posterior thigh; AL: anterior lower leg; PL: posterior lower leg. α vs. boys p < 0.05; β vs. NW boys p < 0.05; γ vs. NW girls p < 0.05.
Figure 2. Muscle thickness and fat thickness outcomes of preschool children. (A) Muscle thickness of boys and girls; (B) Fat thickness of girls; (C) Muscle thickness between NW and OW/OB boys; (D) Fat thickness between NW and OW/OB boys; (E) Muscle thickness between NW and OW/OB girls; (F) Fat thickness between NW and OW/OB girls. NW: normal weight; OW/OB: overweight/obese; UA: upper arm; FA: forearm; AB: abdomen; AT: anterior thigh; PT: posterior thigh; AL: anterior lower leg; PL: posterior lower leg. α vs. boys p < 0.05; β vs. NW boys p < 0.05; γ vs. NW girls p < 0.05.
Children 10 01538 g002
Table 1. Physical characteristics of preschool children.
Table 1. Physical characteristics of preschool children.
ALL a
BoysGirlsSex difference
N = 47N = 39
Age (month)49 ± 649 ± 6
Height (cm)106.6 ± 5.0103.9 ± 5.30.257
Weight (kg)17.9 ± 2.516.7 ± 2.30.370
BMI15.7 ± 1.415.4 ± 1.30.837
Boys a
NWOW/OBBody type difference
N = 38N = 9
Age (month)50 ± 651 ± 6
Height (cm)106.2 ± 5.0108.4 ± 4.60.249
Weight (kg)17.3 ± 1.820.7 ± 3.1p < 0.05
BMI15.3 ± 1.017.5 ± 1.3p < 0.05
Girls a
NWOW/OBBody type difference
N = 34N = 5
Age (month)49 ± 750 ± 3
Height (cm)103.4 ± 5.4107.7 ± 2.90.072
Weight (kg)16.1 ± 1.820.7 ± 0.7p < 0.05
BMI15.0 ± 0.917.9 ± 0.8p < 0.05
Note: Mean ± SD; NW: normal weight; OW/OB: overweight/obese; BMI: body mass index. a Tested with t-test.
Table 2. Daily physical activity outcomes of boys and girls.
Table 2. Daily physical activity outcomes of boys and girls.
BoysGirlsSex
Difference
Daily Difference
Weekday
Daily steps (steps/day)12,185 ± 254910,808 ± 24110.0580.359
MVPA (min/day)39.8 ± 11.236.5 ± 12.00.4820.418
TPA (min/day)124.0 ± 24.4107.8 ± 22.4p < 0.050.535
Weekend
Daily steps (steps/day)11,632 ± 400610,848 ± 50380.465
MVPA (min/day)39.5 ± 18.136.7 ± 24.00.651
TPA
(min/day)
115.9 ± 39.0108.2 ± 46.30.418
Note: Mean ± SD; MVPA: moderate–vigorous physical activity; TPA: total physical activity.
Table 3. Correlation among muscle thickness, fat thickness, and physical activity for boys and girls a.
Table 3. Correlation among muscle thickness, fat thickness, and physical activity for boys and girls a.
BoysGirls
WeekdayWeekendWeekdayWeekend
Daily StepsMVPATPADaily StepsMVPATPADaily StepsMVPATPADaily StepsMVPATPA
Muscle ThicknessUA0.130.020.150.070.040.13−0.18−0.04−0.200.150.200.13
FA0.120.010.14−0.040.010.208−0.12−0.09−0.080.190.210.19
AB0.32 *0.37 *0.320.150.210.140.280.190.310.270.310.25
AT0.240.160.270.110.060.160.100.020.140.220.150.22
PT0.32 *0.200.350.170.120.230.100.080.120.38 *0.35 *0.39 *
AL−0.08−0.13−0.03−0.14−0.05−0.13−0.010.09−0.020.180.230.16
PL0.090.020.140.020.020.060.180.220.160.43 *0.44 *0.43 *
Fat
Thickness
UA−0.13−0.20−0.12−0.06−0.03−0.06−0.01−0.170.04−0.01−0.110.03
FA−0.18−0.28 *−0.14−0.19−0.12−0.18−0.09−0.11−0.090.220.180.24
AB0.04−0.090.090.01−0.060.05−0.07−0.17−0.020.160.060.20
AT−0.14−0.20−0.11−0.09−0.06−0.07−0.27−0.25−0.230.060.020.10
PT−0.05−0.220.01−0.12−0.07−0.11−0.35 *−0.41 *0.30−0.03−0.100.03
AL0.090.010.140.070.080.08−0.28−0.23−0.27−0.02−0.03−0.01
PL−0.15−0.26−0.07−0.14−0.09−0.13−0.31−0.36 *−0.28−0.02−0.100.03
Note: UA: upper arm; FA: forearm; AB: abdomen; AT: anterior thigh; PT: posterior thigh; AL: anterior lower leg; PL: posterior lower leg; MVPA: moderate–vigorous physical activity; TPA: total physical activity; * p < 0.05. a Model 1 was an unadjusted analysis of the muscle thickness, fat thickness, and PA.
Table 4. Correlations among muscle thickness, fat thickness, and physical activity for boys and girls, controlling for years, height, and weight b.
Table 4. Correlations among muscle thickness, fat thickness, and physical activity for boys and girls, controlling for years, height, and weight b.
BoysGirls
WeekdayWeekendWeekdayWeekend
Daily StepsMVPATPADaily StepsMVPATPADaily StepsMVPATPADaily StepsMVPATPA
Muscle ThicknessUA0.070.050.040.150.160.17−0.14−0.01−0.200.140.190.11
FA0.090.030.050.040.110.05−0.05−0.02−0.060.160.170.14
AB0.160.270.180.070.200.010.50 *0.41 *0.48 *0.41 *0.46 *0.39 *
AT0.100.100.090.180.160.190.210.230.200.280.270.27
PT0.39 *0.34 *0.35 *0.280.260.31 *0.41 *0.36 *0.400.340.37 *0.29
AL−0.17−0.09−0.18−0.120.04−0.170.060.23−0.010.080.190.02
PL−0.18−0.08−0.010.060.01−0.060.50 *0.57 *0.44 *0.39 *0.49 *0.33
Fat
Thickness
UA−0.33 *−0.38 *−0.35 *−0.12−0.08−0.14−0.03−0.05−0.01−0.20−0.18−0.18
FA−0.33 *−0.35 *−0.34 *−0.22−0.09−0.26−0.09−0.13−0.090.280.280.29
AB−0.10−0.13−0.120.01−0.050.020.01−0.110.040.08−0.010.12
AT−0.22−0.23−0.22−0.12−0.08−0.12−0.26−0.31−0.22−0.01−0.050.02
PT−0.15−0.03−0.130.13−0.04−0.16−0.48 *−0.49 *−0.45 *−0.09−0.14−0.05
AL0.120.060.160.040.050.05−0.26−0.30−0.230.06−0.010.08
PL−0.21−0.26−0.17−0.11−0.05−0.13−0.39 *−0.43 *−0.35−0.07−0.15−0.03
Note: UA: upper arm; FA: forearm; AB: abdomen; AT: anterior thigh; PT: posterior thigh; AL: anterior lower leg; PL: posterior lower leg; MVPA: moderate–vigorous physical activity; TPA: total physical activity; * p < 0.05. b Model 2 was adjusted for height, weight, and duration of daylight.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Deng, P.; Ozaki, H.; Natsume, T.; Ke, D.; Lu, D.; Suzuki, K.; Naito, H. Associations of Morphological Changes in Skeletal Muscles of Preschool Children in China Following Physical Activity. Children 2023, 10, 1538. https://doi.org/10.3390/children10091538

AMA Style

Deng P, Ozaki H, Natsume T, Ke D, Lu D, Suzuki K, Naito H. Associations of Morphological Changes in Skeletal Muscles of Preschool Children in China Following Physical Activity. Children. 2023; 10(9):1538. https://doi.org/10.3390/children10091538

Chicago/Turabian Style

Deng, Pengyu, Hayao Ozaki, Toshiharu Natsume, Dandan Ke, Dajiang Lu, Koya Suzuki, and Hisashi Naito. 2023. "Associations of Morphological Changes in Skeletal Muscles of Preschool Children in China Following Physical Activity" Children 10, no. 9: 1538. https://doi.org/10.3390/children10091538

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop