Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study.

We compared the motor competence between overweight/obese and eutrophic preschoolers with similar physical activity levels, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment. We also investigated to what extent excess body fat mass explains gross motor skills in preschoolers. A cross-sectional quantitative and exploratory study was conducted with 48 preschoolers assigned into eutrophic and overweight/obese groups. Overweight/obese preschoolers had worse Locomotor subtest standard scores than the eutrophic ones (p = 0.01), but similar Object Control subtest and Gross Motor Quotient scores (p > 0.05). Excess body fat mass explained 12% of the low Locomotor subtest standard scores in preschoolers (R2 = 0.12; p = 0.007). Excess body fat mass was associated with worse locomotor skills when the model was adjusted for physical activity levels, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment. Thus, excess body fat mass partly explains lower locomotor skills in preschoolers.

Introduction

Childhood obesity is a growing public health concern worldwide [1]. In the past decades, childhood obesity was considered a problem, especially in developed countries, but recent evidence indicates the rapid growth of obesity in children from developing countries. [2, 3]. Epidemiological data point to the comorbidities related to excess body fat mass, such as impaired glucose tolerance and hepatic steatosis [4], as the main responsible for the childhood obesity pandemic [1, 5]. In Brazil, among children under 5 years of age, 14.8% are overweight and 7% are obese [6].

Early childhood, especially the preschool period between 3 to 5 years [7], is the stage of life when the body mass index (BMI) is reduced to a minimum physiological value known as adiposity rebound [8]. Studies indicate that weight gain during preschool years (but not during school years) is associated with a risk of overweight or obesity in adolescence, a factor that characterizes this phase as sensitive for preventing excess body fat mass [8]. Moreover, it is also considered a sensitive phase for learning fundamental movements; it is a time to expand the motor repertoire and experience the movements that will contribute to the development of future skills that will evolve into sports or leisure practices [9]. Studies indicate the preschool period as the critical moment for the development of motor skills and healthy behaviors that may influence physical activity (PA) practices throughout life [10, 11].

Regarding the impact of childhood obesity on the development of children, a previous study of our team, including 6 to 24 months overweight and obese infants, evidenced that although overweight and obese infants presented a development within a normal range, they had a worse motor and cognitive skills [12]. Of note, the analyses performed in this previous study considered factors that could interfere with child development, e.g., socioeconomic status, mother education, resources of the domestic and yard environment [12].

Although previous work has shown that fat mass was not related to any motor skill measure [13], other studies have found an association between overweight/obesity with low motor competence (MC) in children [10, 12, 14–16], including a work with Brazilian preschoolers from the Northeast region of Brazil [15] and longitudinal studies [17-19]. However, to our knowledge, there remains a gap regarding the association between overweight and obesity with motor competency, specifically in children with preschool age.

In addition, other factors beyond obesity, such as socioeconomic status [20, 21], culture and/or geographical location [22], mother education [23, 24], resources of the domestic environment [25], resources of the school [26] and PA levels [27-30], may influence gross MC. Thus it is crucial to match groups concerning these factors to avoid interpretation bias.

In a systematic review [31] focusing on obesity in Brazilian children, the authors stated that although there has been an increase in publications in recent years, well-controlled studies regarding the association between overweight/obesity and MC are still scarce. Furthermore, studies have failed to provide information about sample size, variance and effect estimates, statistical power, and adjustment of possible confounders in data analysis [32]. Moreover, because most of the studies include children in a wide range of age and at many stages of biological maturation [33], the results are inconclusive, limiting the validity, interpretation and extrapolation of the results for preschoolers [31]. These studies also present different methods to measure excess body fat mass, e.g., BMI [33], waist-hip circumference [15], or body fat mass measured with bioelectrical impedance [29]. Thus, to the best of our knowledge, none of these studies have measured body fat mass using dual-energy radiological absorptiometry (DEXA), the gold standard for body fat mass measurement.

In light of the above, is excess body fat mass (measured by a gold-standard method) in preschoolers associated with worse gross motor skills when matched for socioeconomic status, home and school environment, maternal education and PA levels?

The aim of this study was: 1) To compare the gross MC between overweight/obese and eutrophic preschoolers according to PA levels, sex, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment. 2) To investigate to what extent excess body fat mass explains gross motor skills in preschoolers.

Materials and methods

This is a quantitative, exploratory, cross-sectional study approved by the Research Ethics Committee of Universidade Federal dos Vales do Jequitinhonha e Mucuri UFVJM (Protocol: 2.773.418). Data collection took place from July to December 2019. The inclusion criteria were preschoolers aging 3 to 5 years old from public schools in a Brazilian municipality. This study was part of a larger project linked to the municipal education department that included a large database of overweight and/or obese children. Parents of preschoolers from this database were contacted and invited to participate in the study. In total, seventy parents were contacted, and sixty-six agreed to participate in the study. Exclusion criteria were children who had incomplete data in the database; preterm and low birth weight infants and infants with pregnancy or parturition complications; children with signs of malnutrition or illness that interfere with growth and development or any disability; children who were at risk of being overweight or underweight and children affected with any infection during the study period (e.g., fever, influenza, or diarrhea).

The sample size was based on a pilot study with five children in each group. For sample size calculation, we used the Standard Score Locomotor of the TGMD2 and found an effect size of 0.94 using a minimum difference of 2.70 between the groups, with a standard deviation (SD) of 3.50 (G1 = 20.1, SD ±4.30 and G2 17.4, SD± 2.70). In addition, we considered a power of 90% and an alpha error of 5%, totaling 40 participants (20 participants/ group). Forty-eight preschoolers from the database were eligible to participate in this study. All participants were previously informed of all procedures of the study during a home visit by a researcher.

Weight and height measurements were taken during the study visits. The children’s weight was measured to the nearest 0.1 kg using an electronic scale and height was measured to the nearest 0.5 cm using a stadiometer. The children removed their shoes and socks before stepping on the scale and were told to stand in an upright position when measuring weight and height. BMI was calculated using body weight (kg) divided by body height squared (m2) and the child’s birth date was also considered to the final BMI index according to the World Health Organization software [34].

Considering the high correlation between body fat mass and BMI (r = 0.90, p = 0.00), the participants were classified into groups according to BMI, following World Health Organization (WHO) recommendations. The WHO reference curves by gender and age were considered using the WHO Anthro version 3.2.2 software [34]. According to WHO guidelines, weight-for-length/height Z score should be used to assess body weight in children under five years old. Children with a BMI <1SD were considered eutrophic and assigned to Group 1, whereas children with a BMI ≥ 2SD were considered overweight or obese and assigned to Group 2.

Age, socioeconomic status, maternal education [35], PA [29], quality of the home environment and quality of the school environment [24] were collected for control. The ICC test-retest reliability of all the questionnaire used were over 0.90.

The Brazil economic classification criterion from the Brazilian Association of Research Companies was used to verify the economic status of families. This is a questionnaire that stratifies the general economic classification from A1 (high economic class) to E (very low economic class) status [36].

Home Observation for Measurement of the Environment. Inventory—Early Childhood (ECHOME). The EC-HOME [37] is an instrument for observation and measurement of the family environment. The Early Childhood (EC) version is directed at children aged three to six years. The application of the instrument is carried out through a visit that includes observation and the performance of an interview with the people responsible for the child. The instrument consists of 55 items, which are divided into eight subscales: 1—Learning Materials; 2—Language Stimulation; 3—Physical Environment; 4—Responsivity; 5—Academic Stimulation; 6—Modeling; 7—Variety; and 8—Acceptance. Of the 55 items, 21 are based on observation of the family environment, 10 on observation and 24 on an interview, preferably with the mother. Each item in each domain is scored dichotomously (0 or 1), with a maximum score of 55 points (high scores reflect better evaluation in each domain). The sum of the raw scores of the subscales was used for analyses. The HOME Inventory has been used worldwide to evaluate the home environment in both international [38] and transcultural studies [39], presenting psychometric characteristics investigated in Brazilian preschoolers (Cronbach’s Alpha = .84 for the 55 items) [40].

The quality of the school environment was assessed using the Early Childhood Environment Rating Scales (ECERS) [39], a global measure of the quality of early education for preschoolers from 2 to 5 years of age. The ECERS-R consists of 43 items divided into seven subscales (1-Space and Furnishings, 2-Personal Care Routines, 3-Language and Literacy, 4-Learning activities, 5-Interactions, 6-Program Structure, 7- Parents and staff), that are scored during live observations. A value between 1 and 7 (Likert scale) is given to each of these subscales ranging from inadequate to excellent. Then global scores are calculated based on the averages of all items. Following the standard instrument guidelines, the final score is classified as inadequate care (1.00–2.99), adequate care (3.00–4.99), or good to excellent care (5.00–6.99; Harms et al., 2013) [41]. This questionnaire is a well-known international instrument translated to the Portuguese language [42] and used by different Brazilian studies [42-44] with established psychometric properties for Brazilian preschoolers [45].

The PA level was measured using an accelerometer (Actigraph®- Model GT9X); for three valid days (excluding weekends) [46], for a minimum of 570 minutes per day [29], which is considered suitable for preschoolers [47]. Accelerometers were initialized and analyzed using 5-second epochs. In all analyses, consecutive periods of ≥ 20 minutes of zero counts were defined as non-wear time [46], with a sampling rate of 60 Hz. The accelerometer was positioned on the right side of the hip to capture accelerations and decelerations of the body and determine objective measurements of gross acceleration, PA intensity, intervals and the total time of suspension of use [46]. The classification adopted for “active” or “insufficiently active” was established according to the WHO, which considers an active child the one who has PA levels of at least 180 minutes/day, being at least 60 minutes/day of moderate to vigorous PA [48]. Then, pediatric cutoff points validated for preschoolers were used to classify the children’s PA levels as insufficient (0 to 819 counts / m), mild (820 to 3907), moderate (3908 to 6111) and vigorous (above 6612)PA levels [49]. A trained researcher placed the device on the child’s hip at 7 a.m. and the person responsible for the child was instructed to remove it at 7 p.m. If necessary, a new collection took place in the following week. The average time was calculated considering the simple average of the valid data.

MC was measured using the Test of Gross Motor Development second edition (TGMD-2). The reference is based on a criterion for children between three and ten years old. The TGMD-2 consists of 12 motor skills divided into two categories: 1. locomotor (run, leap, gallop, hop, jump and slide); and 2. object control (catch, strike, bounce over and underhand throw, and kick). For each skill, specific motor criteria are observed based on mature movement patterns referenced in the literature and by professionals in the field. The results obtained for each subtest are added, and the raw scores are converted into normalized scores for sex and age with a mean of 100 ± 15 [50], validated for Brazilian children [51]. For the study, the standardized scores described in Standard Score Locomotor (LP), Standard Score Object Control (OC) and Sum of the Gross Motor Quotient (GMQ- which includes the LP and OC) were used. The subtest standard scores are combined and converted to an overall Gross Motor Quotient (GMQ), determining a child’s gross motor skills compared to the tests from the standardized population. For this study, each subscale of the test (LP and OC) and the GMQ were used as dependent variables for statistical analysis. The reliability for TGMD2 showed intra-class correlation coefficients (ICC) of 0.895 for the LP, 0.925 for OC and 0.841 for GMQ. The tests were applied at the Exercise Physiology laboratory from the Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM), with footage of the participants for later scores by the examiner. A recent systematic review [52] indicated that, regardless of the test variation, the TMGD has moderate-to-excellent internal consistency, good-to-excellent inter-rater reliability, good-to-excellent intra-rater reliability, and moderate-to-excellent test-retest reliability.

The EC-HOME questionnaire [37] was applied at the child’s home, the ECERS [41] at the school where the child studied and the other tests were applied at the Exercise Physiology laboratory from the Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM). All tests and measurements, including body weight, height, assessment of gross MC, as well as questionnaires, were applied by a trained examiner. The children were evaluated following a previously defined order, with an interval between data collection of a maximum of 3 weeks.

The data were analyzed using the Statistical Package for the Social Sciences (SPSS version 2.2). First, the Shapiro-Wilk (SW) test was performed to assess data normality, followed by Levene’s test to verify the homogeneity of the variance. The descriptive statistics of continuous variables were expressed as median (minimum and maximum) or mean ± standard deviation. A Chi-square test was applied to compare the frequency of children in the eutrophic and overweight/obese groups. The t-test for independent samples (for variables with normal distribution) or the Mann-Whitney test (for variables with non-normal distribution) was used to verify differences between groups.

Spearman’s or Pearson’s correlation was performed to verify the relationship between body fat mass and gross motor competence, followed by the simple linear regression model between independent variables and the dependent variable LP. Variables with p<0.2 was included in the multiple linear regression model analysis (stepwise). Statistical significance was set at 5%.

Results

Table 1 presents the sample characteristics. Forty-eight children (24 eutrophic and 24 overweight) were evaluated. Among the children with excess body fat mass, 17 (70.8%) were obese and 7 (29.2%) were overweight.

Table 1

Sample characteristics.

Variable	Eutrophic	Overweight	Test	p-value
	N = 24	N = 24
Age (years)	4.58 ±0.58	4.68±0.64	1.151.0b	0.627
Sex N (%)			0.19 c	0.656
Female	11(45.8)	10(41.7)
Male	13(54.2)	14(58.3)
Mother’s age (years)	30.96 ±6.09	31.88 ± 5.81	21.51b	0.306
Economic status N (%)			224.50 a	0.171
B	4(16.7)	9(37.5)
C	18(75.0)	13(54.1)
D-E	2(8.3)	2(8.3)
Maternal Education N (%)			279.50 a	0.841
Primary	3(12.5)	5(20.8)
Secondary	17(70.8)	12(50.0)
Higher	4(16.7)	7(29.1)
Amount of body fat mass (kg)	4.02±1.11	10.89±2.96	1.00 a	<0.001
Mean Intensity of PA(minutes/day)
Sedentary	398.42±41.67	397.74±46.42	0.04b	0.965
Light PA	190.34±37.68	185.08±32.94	0.51 b	0.612
Moderate PA	37.33±10.93	42.02±9.51	-1.43 b	0.158
Moderate to Vigorous PA	59.17±15.45	61.09±14.30	-0.34 b	0.186
Classification of PA N (%)			0.18c	0.448
Active	12 (50)	14 (58.33)
Insufficiently active	11 (45.8)	10 (41.66)
EC-HOME (point)	37.91±4.79	40.75±5.90	209.0a	0.102
Quality of the school environment (ECERS) (point)	2.58±0.28	2.58±0.29	271.0a	0.725

Data presented by mean ± standard deviation, median (min-max). PA: Physical Activity. EC-HOME: Early Childhood Home Observation for Measurement of the Environment. ECERS: Early Childhood Environment Rating Scales.

a Mann-Whitney U Test.

b T-test for independent samples.

C chi-square test.

The mean age in both groups of preschoolers was 4.5 years (±0.6). Most of the children belong to extract C in the economic classification. In both groups, there was a predominance of young adult mothers with completed high school education. More than half of the preschoolers attended part-time schools with a playground and other physical space for PA practices. Regarding the home environment stimulation, in the eutrophic group, 23 (95.8%) children lived in medium stimulation environment and 1 (4.2%) lived in high stimulation environment; in the overweight group, 16 (66.7%) children lived in medium stimulation environment, while 8 (33.3%) lived in high stimulation environment (Table 1).

There was no difference between groups for variables that influence children’s motor behavior (age, sex, economic status, maternal education, PA, EC-HOME, quality of the school) and others that characterize them, demonstrating the pairing of the sample. As expected, the amount of body fat mass was different between the groups (p value <0.001) (Table 1).

The comparison between groups for Motor Competence are found in Table 2.

Table 2

Comparison between groups for motor competence.

	Eutrophic (N = 24)	Overweight (N = 24)	Difference between groups*	p-value	95%CI
TGMD2 LP	9.04±1.89	7.63±2.08	2.46	0.018	0.25–2.57
TGMD2 OC	8.88±2.69	8.33±1.73	0.823	0.412	-0.77–1.85
TGMD2 GMQ	93.38±11.17	83.54±9.09	1.98	0.053	-0.08–11.75

Data presented by Mean ±standard deviation or median (Minimum-Maximum).

*T-test for independent samples. Abbreviations: TGMD2 LP = Standard Score Locomotor. TGMD2 OC = Standard Score Object Control, TGMD2 GMQ = Gross Motor Quotient.

There was no difference between groups for OC subscales and GMQ. A significant difference was found in the LP between the groups; compared with the normal-weight group, the overweight/obese group had lower LP scores (Table 2). The post-hoc analysis, considering an effect size of 0.70 (alpha value = 0.05), revealed a large statistical power for the LP (Power = 0.96).

For OC there were no significant values (data presented in S1 Data). The amount of body fat mass was negatively correlated with the LS score (Pearson’s correlation; r = -0.38, p-value = 0.007).

Table 3 presents data from simple linear regression. Age and body fat mass presented a p value < 0.2 and was included in the multiple linear regression model analysis. Body fat mass showed significance with LP (p = 0.007). The multiple linear regression is presented in Table 4.

Table 3

Regression between independent variables and standard locomotor score.

(N = 48).

	Simple linear regression
	Locomotor subset standard score
Variable	ẞ	B	95% CI	p-value	R2
Classification of PA	0.140	0.590	-0.66-(1.84)	0.348	-0.002
Sex	0.614	-0.423	-1.65-(0.81)	0.494	0.010
Age (years)	-0.211	-0.725	-1.72-(0.27)	0.150	0.024
Economic status	0.177	-0.348	-0.22-(0.92)	0.228	0.010
EC-HOME (point)	0.067	0.026	-0.08-(0.13)	0.649	-0.005
Quality of the school environment (ECERS) (point)	0.055	0.401	-1.76-(2.56)	0.711	0.003
Body fat mass(kg)	-0.382	-0.195	-0.334-(-0.055)	0.007	0.146

Note: ẞ = standard regression coefficient; B = non-standard regression coefficient; 95% CI = 95% confidence interval; estimate of the increase or decrease of the dependent variable for each increase of one unit of the independent variable; p = statistical significance; R2 = coefficient of determination. PA: physical activity. EC-HOME: Early Childhood Home Observation for Measurement of the Environment. ECERS: Early Childhood Environment Rating Scales.

Table 4

Multiple linear regression.

Standard Score Locomotor
Variable	ẞ	B	95% CI	p-value	R2
Body fat mass	-0.382	-0,195	-0.33– (-0.05)	0.007	0.12

Note: ẞ = standard regression coefficient; B = non-standard regression coefficient; 95% CI = 95% confidence interval; estimate of the increase or decrease of the dependent variable for each increase of one unit of the independent variable; p = statistical significance; R2 = coefficient of determination

Multiple linear regression analysis showed that there was an inverse relationship between body fat mass and LP. The high body fat mass explained 12% of the low values in the LP scores in preschoolers. Specifically, for each 1 kg of body fat mass increase, it is expected a 0.19 points decrease in the LP score, with a medium effect size (d = 0.16) (Table 4).

Discussion

This study aimed to compare the MC between overweight/obese and eutrophic preschoolers matched for PA levels [29], age, socioeconomic status, maternal education [35], quality of the home environment and quality of the school environment [24]. Identifying variables that may interfere with child development has an important clinical relevance since the child’s reciprocal relationships with the environment can influence child development [24, 53]. We believe that these variables did not impact the MC due to the similarities between the groups with regard to by variables described (Table 1) with non-significant p-value (p> 0.05).

The preschoolers of both groups were selected from public schools in the same municipality (Diamantina city, Minas Gerais, Brazil). Of note, the methodology of the present study followed the same methodology from our previous study, also developed with infants [12]. Excess body fat mass was the only factor associated with the worst MC in preschoolers. To the best of our knowledge, this is the first study comparing MC between eutrophic and overweight/obese preschoolers using robust methods for measuring PA levels (accelerometers) and body fat mass content (DEXA). Moreover, we collected some critical data that may interfere with the motor development in preschoolers, i.e., socioeconomic status, maternal education [35] and the quality of the home and school environment. Regarding the home environment, we evaluated the availability of resources and toys, trips and opportunities for stimulating experiences, use of free time, family routines and meetings, physical space of the home environment and the direct involvement of parents in the child’s life [24, 37].

The excess of body fat mass appears as a factor that interferes with MC in LP. Being overweight/obese seems to hinder displacements since antigravity activities are more difficult [33, 54] due to the morphological restrictions to movement within high biomechanical restrictions that make it more challenging to perform tasks involving changes in the center of mass [16]. Other studies [53, 55] have also found an inverse relationship between excess body fat mass and motor skills in preschoolers [16, 29]. Studies with Brazilian children (3 to 5 years old) used the same motor tests as in the present study and also found an inverse relationship between body fat mass and LP scores [15].

Excess body fat mass is associated with worse MC [17, 18, 32, 56, 57], as overweight/obese seems to contribute to declines in motor proficiency. Despite previous study [56], investigating temporal precedence in the relationship between MC and weight status in schoolchildren aged between 5 and 10, found poor MC did not predict weight gain, the literature is conflicting. Although previous work has shown that fat mass was not related to any motor skill measure [13], according to Lima and colleagues [18], poor MC at 6 years old seems to be associated with excess body fat mass during childhood [18].

Our data revealed an inverse association between excess body fat mass and MC. Here, the excess body fat mass explained 12% of the worse LP scores in preschoolers. Thus, the present study results reveal strong evidence of a negative association between excess body fat mass and MC [33] and the relative declines in children’s motor proficiency can serve as a catalyst for inactivity and consequent weight gain with advancing age [10, 53]. In this sense, we emphasize that this relationship can be bidirectional from a preschool age [15].

This study has some limitations and strengths. The sample was small; however, the sample size was sufficient to achieve a medium to large effect size. The study has a cross-sectional format, which does not allow inferring a cause-and-effect relationship; then, longitudinal studies are necessary to examine the development of MC and its relationship with other health-related outcomes. However, to our knowledge, this is the first well-controlled study investigating the influence of excess body fat mass on MC in preschoolers. Among the strengths of this study, we highlight the short data collection interval (maximum of three weeks), the use of a standardized instrument for assessing MC [50], the use of a TGMD2 test validated for Brazilian children [51], the direct measurement of PA levels with accelerometer [29], and the use of DEXA, a gold-standard method to measure body fat mass [58]. Finally, we also highlight the assessment of relevant factors that interfere in the child’s motor development [24, 29], i.e., socioeconomic level of the family, maternal schooling [35], quality of the school environment [24, 46] and quality of the home environment [24, 37].

Conclusions

The excess body fat mass is associated with worse locomotor skills in preschoolers even when even when matched for other important variables that can interfere with MC. These findings point to the importance of developing strategies to increase preschoolers’ motor competence (especially locomotion skills) and reduce excess body fat mass in preschoolers.

• Preschoolers with excess body fat mass have worse locomotor skills than eutrophic preschoolers even when matched for maternal education, socioeconomic status, PA, sex, age, quality of the home environment and quality of the school environment.

• The worst locomotor skills in preschoolers with excess body fat mass reveal the importance of strategies to stimulate locomotor skills, especially in the context of pediatric obesity.

(XLSX)

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Regression between independent variables and standard score object control (N = 48).

(DOCX)

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13 Oct 2021

Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study

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Reviewer #1: Review Ms PONE-D-21-16031

Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study.

The authors compared motor competence in a relatively small sample of overweight/obese and eutrophic children (5 yrs of age), thereby taking a series of secondary variables (PA, sex, gender, age, SES, etc…) into account. While the underlying rationale of the study is to be applauded, and the authors collect an impressive set of variables with state-of-the-art assessment instruments (great effort, much appreciated!!!), the writing of the paper itself is problematic and unacceptable for publication in this form. I had the impression that this paper was written under severe time pressure, resulting in a kind of ‘quick & dirty job’.

I hope that my comments in attachment are helpful for the authors to rework this material that does have publication potential, but not in its current form.

Reviewer #2: The manuscript entitled “Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study” compared the motor competence of overweight/obese preschoolers with eutrophic peers. Overall, the manuscript is well written and it approaches an important topic regarding child health. However, there are some issues in this work which should be better addressed by the authors. Both general and specific comments are provided as per below.

General comments

Literature provides extensive evidence about the relationship between motor competence and weight status across childhood, yet the background provided by the authors is little informative. As such, it is not clear what is already known about the relationship between body fat and motor competence in preschool children. In addition, the authors argued that “the strength of the present study is the consideration of multiple factors that influence child development” (page 4). However, it is not clear the rationale for considering these multiple factors (i.e. PA, sex, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment) as potential confounders. In addition, it does not seem appropriate to consider “factors that influence child development” in a cross-sectional study.

Also, this cross-sectional study has a small sample size, especially when considering the multiple factors/variables inserted in the regression analysis.

Specific comments

Introduction

- Overall, I would suggest to provide a focused background considering the relationship between weight status and motor competence across childhood. This seems the main focus of this study and as such it should be better presented in the Introduction.

- The state of knowledge about the relationship between weight status and motor competence is missing. Please, provide a more detailed background and explain the ‘why’ we should consider “PA, sex, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment” as potential confounders.

Methods

“For sample calculation, a power of 90%, and an alpha error of 5% were considered, with 20 participants thus being required for each group, totaling 40 subjects.” (page 5, 2nd paragraph).

And the effect size? Did you calculate the sample size considering the number of total predictors and the effect size?

Results

In the Table 3, there two regression models (i.e. pre- post adjustment). Please, explain this analysis in the Methods section.

Discussion

I think the Discussion should be reassessed by the authors considering the previous comments.

**********

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Submitted filename: Review Ms PONE.pdf

Click here for additional data file.

18 Nov 2021

Ref: PONE-D-21-16031

Title: Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study

PLOS ONE

Dear Avanti Dey, PhD

Staff Editor

PLOS ONE

We appreciate the reviewer’s comments. They were important to improve the quality of our manuscript. See below the point-to-point answers.

PONE-D-21-16031

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

Answer: We have made the requested adjustments.

2. Please state whether you validated the questionnaire prior to testing on study participants. Please provide details regarding the validation group within the methods

Answer: The ICC test-retest reliability of all the questionnaires used was over 0.90 (see line 136). We enter the psychometric properties of the instruments used in the Methods session

3. Thank you for submitting the above manuscript to PLOS ONE. During our internal evaluation of the manuscript, we found significant text overlap between your submission and the following previously published works, some of which you are an author.

- https://www.researchsquare.com/article/rs-612416/v1

- https://www.researchgate.net/publication/283530031_Test_of_gross_motor_development-2

- https://www.frontiersin.org/articles/10.3389/fphys.2019.01273/full (last paragraph of discussion)

We would like to make you aware that copying extracts from previous publications, especially outside the methods section, word-for-word is unacceptable. In addition, the reproduction of text from published reports has implications for the copyright that may apply to the publications.

Please revise the manuscript to rephrase the duplicated text, cite your sources, and provide details as to how the current manuscript advances on previous work. Please note that further consideration is dependent on the submission of a manuscript that addresses these concerns about the overlap in text with published work.

Answer: We have made the requested adjustments. The description of the TGMD2 test has been duly cited (see URICH, 2000). Of note, Plos One team encourage to researchers to submit their manuscript to a preprint server directly (https://plos.org/open-science/preprints/preprint-faqs/). Thus, we have made a preprint submission. In addition, despite our team having another study (https://www.researchsquare.com/article/rs-612416/v1) in line with the present study, they are very different, including the question. With this regard, we have used an anti-plagiarism software Copyspider (Copyspider), obtaining a value of 2.43% (up to 3% is acceptable). Finally, we have carefully reviewed the manuscript before resubmission.

Reviewer #1:

Review Ms PONE-D-21-16031

Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study.

We thank the reviewer for the comments and suggestions; they helped improve the quality of our manuscript further.

Language: This manuscript needs a thorough revision by a native English speaker or by a professional familiar with the writing of scientific reports.

Answer: All the authors, some of them living abroad, have carefully reviewed the English language.

Abstract: • Use the same tense during the abstract • ‘quantitative’: how to be interpreted here? Should be quantitatively? • Sentence with ‘but similar skills’… check grammar • Globale language revision is mandatory

Answer: We have corrected the tense and grammar throughout the text.

Introduction: • The introduction is too short and superficial to allow the development of a solid rationale for this study. Specifically with respect to the weight/motor skill relationship, the authors can start from the abundance of literature in children from 5 years and older, describe what we know already in more detail (point to the urgency of the problem), and then move on tot he part in which the paucity of similar studies in younger children is described. This approach will also help to formulate specific hypotheses at the end of the introduction. You may want to consults the publications of Eva D’Hondt / Mireille Augustijnen between 2008-2010 for that purpose.

Answer: We agree with the reviewer’s comment. Because of the lack of studies with preschoolers, we have adjusted the introduction session to bring theoretical references, providing the basis for understanding how far the literature has advanced the relationship between motor competence and body fat in children. We emphasize that we were careful to pair preschool children in both groups considering the variables influencing child development and could cause interpretation bias in the primary variables (see the previous study of our team including infants up to 2 years of age, Camargos et al., 2016). (See lines 44-50; 64-68; 69-78; 82-83.)

• I applaud the inclusion of the impressive set of secondary variables, but the rationale on why to include one variabele (and not other ones) is lacking. Suggestion to shortly describe for each of the variables whether they might have a positive or a negative effect on motor competence. Again, this will help building a solid set of hypotheses.

Answer: We have improved the introduction session according to the reviewer's suggestion. (See lines 44-50; 64-68; 69-78; 82-83).

• Describing the strength of the study does not belong at the end of the introduction

Answer: We have removed this sentence from the end of the introduction session.

Methods: • More information on the recruitment procedure is needed. How many parents were contacted for each group and how many agreed participation of their child?

Answer: We have included additional information on the recruitment procedure (see lines 105-106).

• I assume you mean that you excluded participants that were subject to an infectious process at the time of the study (not …had been subject..)? ]

Answer: Yes! We have excluded participants that were subject to any infectious process during the study. We included this information in the text (see line 110). “overweight or underweight and children affected with any infection during the study period …”

• I agree that the sample size is large enough for the straightforward comparison between groups, but did the authors also reck on with the extended set of secondary variables in their power analysis?

Answer: Although we have adjusted the final model for all variables that could interfere with the result, only "body fat mass" remained as an independent variable associated with “Standard Score Locomotor” in the model (Table 4). With this regard, we have performed the post hoc power analysis and obtained a medium effect size (d = 0.16) and a power of 0.77 (see Lines 282-285).

Print Screen:

• How is age-specific BMI age specific as you just calculate weight/m²? Please be more specific.

Answer: To calculate the BMI, we have used a software from the World Health Organization considering the age and the child's weight and height. We have inserted this additional information and reference (see ref 32: WHO, 2011).

Lines 125-126: Age-specific BMI was calculated using a specific World Health Organization software. Of note, the calculation considered the child's date of birth and data on body weight (kg) divided by body height squared (m2).

• Please provide reliability/validity information on each test instrument.

Answer: We have provided reliability/validity information on each test instrument in the text as follows.

HOME: (See lines 153-156): The HOME Inventory has been used worldwide to evaluate the home environment in both international [36] and transcultural studies [37], presenting psychometric characteristics investigated in Brazilian preschoolers sample, analysis of internal consistency satisfactory for the total scale (Cronbach's Alpha = .84 for the 55 items) [38].

ECERS: (See lines 166-168): This questionnaire is a well-known international instrument translated to Portuguese [40] and used by different Brazilian studies with preschoolers [40; 41; 42] with established psychometric properties for Brazilian preschoolers [43].

TGMD2: (See lines 203-206): Recent study systematic review [51] indicated that, regardless of the variant of the test, the TMGD has moderate-to-excellent internal consistency, good-to-excellent inter-rater reliability, good-to-excellent intra-rater reliability, and moderate-to-excellent test-retest reliability.

• ACtigraph: more details are needed. Were the 3 days randomly chosen? Weekdays and/or weekend days? Please first describe the instrument, then how it is positioned, and then information on the analysis. Not clear how you can capture heart rate with a hip-mounted device. How is ‘the child’s mean time’ calculated?

Answer: We have included additional information about ACtigraph measures.

(See line 170): three valid days (excluding weekends)

(See lines 181-185): A trained researcher placed the device on the child's hip at 7 a.m. and the person responsible for the child was instructed to remove it at 7 p.m. If necessary, a new collection took place in the following week. The average time was calculated considering the simple average of the valid data.

.• TGMD-2: 12 motor skills divided into two categories (not subtests)

Answer: Yes! We have modified accordingly (see line 188): divided into two categories

• Data are presented as mean or median, as appropriate. I assume you mean ‘depending on the outcome of the SW and L test. See comment under results.

Answer: We have performed new statistical analyzes and restructured the data presentation (see table 1). Noteworthy, both KH and SW have the same distribution (non-normal) for the dependent variable. We have adjusted the data presentation according to this distribution.

• The statistics section lacks structure, and this reflects in the Tables. It is very hard to figure out what test was use for what variable from the tables. I am not convinced that it is necessary to strictly adhere to the results of the SW and L test to decide on the statistical approach for each variable independently given the –in my opinion-sufficiently large number of participants per group.

Answer: We have performed new statistical analyses and adjusted the text (see lines 222-224). “Spearman's or Pearson’s correlation was performed to verify the relationship between body fat mass and gross motor competence variables, followed by the simple linear regression model between independent variables and the dependent variable LP. Variables with p<0.2 became part of the multiple linear regression model (stepwise).Statistical significance was set at 5%.”

Results:

• Table 1: please provide the units for each variable (eg under ‘sex’ it is N, with the proportion in brackets; is amount of body mass in kg or a %; etc.)

Answer: We have provided the units for each variable in table 1 (highlighted in the text).

• Subscript ‘a’ is floating in the table, where does it belong to? • I would say that children this age ‘attend’ school rather than ‘study’

Answer: We have modified accordingly (highlighted in the text).

• Of course it makes sense that body mass differed between groups, given that children were selected on being overweight.

Answer: We have performed new statistical analyses (n=48, 24 in each group), clarifying a strength of our study since we collected data of variables that could lead to an interpretation bias.

Thus, the strict internal control of our study enabled the comparison between the locomotor skills of preschoolers in similar conditions of child development, except for excess body weight. Now, we hope it is clear throughout the text.

• Table 2: mixing between parametric and non-parametric stats in subscores of the same test battery is confusing

Answer: Yes! We agree with this reviewer’s comment. We have made the adjustments in table 2.

• Please provide also the results of the OC analyses. Not finding significant differences is as important as reporting the significant ones!

Answer: We have inserted the results of the OC analyses as a supplementary file. We also have included a paragraph about OC results in the results section.

Line 261: For OC there were no significant values (data presented in supplementary material).

Discussion: • The last paragraph of the results is confusing: first you mention the MLR adjusted for confounding factors. You end the paragraph with …’Finally, control variables were inserted in the model….’ Isn’t that twice the same?

Answer: We agree with this reviewer’s comment that we have already mentioned that the control variables were inserted (adjusted) in the regression model. We have excluded this sentence from the results session.

• The participants were selected from public schools in the same municipality, which might explain the absence of differences in the secondary variables? Discuss where this group is to be situated compared to rest of the Brazilian children?

Answer: We have included in the discussion session the requested information as follows:

(see lines 296-299): The preschoolers of both groups were selected from public schools in the same municipality (Diamantina city, Minas Gerais, Brazil). Of note, the methodology of the present study followed the same methodology from our previous study, also developed with infants [11]. Excess body fat mass was the only factor associated with the worst MC in preschoolers.

• The results could be better framed within the knowledge on children that are slightly older. For example, several studies did find differences in fine motor skills in young obese children (I think D’Hondt et al in Neuroscience Letters or APAQ somewhere in 2008 or 2009). Might be worthwile discussing in a broader context.

Answer: We have included additional information from recent studies investigating motor skills in young obese children (see lines 317-326):

“Excess body fat mass is associated with worse MC [15;16;54;55;30], as overweight/obese seems to contribute to declines in motor proficiency. Despite previous study [54], investigating temporal precedence in the relationship between MC and weight status in schoolchildren aged between 5 and 10, found poor MC did not predict weight gain, the literature is conflicting. Thus, according to Lima and colleagues [16], poor MC at 6 years old seems to be associated with excess body fat mass during childhood [16].

Our data revealed an inverse association between excess body fat mass and MC. Here, the excess body fat mass explained 12% of the worse LP scores in preschoolers. Thus, the present study results reveal strong evidence of a negative association between excess body fat mass and MC [30]

• On p 14, I cannot understand why the concept of ‘body image’ suddenly emerges in the discussion. Difficult sentence to grab, please clarify.

Answer: Yes! We have excluded this information.

• You may want to consult the recent meta-analysis by Barnett et al in Sports Medicine (2021), overviewing among others the longitudinal relationship / causality between weight status and MC (and the reverse).

Answer: Thanks to the reviewer! We have included additional information to improve the discussion session.

In addition, lines 324-326 “Thus, the results of the present study add to the current literature, as showed a strong evidence of a negative association between excess body fat mass and MC [30]”

• Near the end of the discussion and practical implications: suggestion to stick to the findings of this study. This was a cross-sectional study, so the conclusion that excess body fat mass influences competence in locomotor skills should be toned down a bit.

Answer: We have modified the conclusion session as suggested (see lines 342-346).

The excess body fat mass is associated with worse locomotor skills in preschoolers even when even when matched for other important variables that can interfere with MC. These findings point to the importance of developing strategies to increase preschoolers' motor competence (especially locomotion skills) and reduce excess body fat mass in preschoolers.

.• The practical implications do not relate to the findings of this study at all, please revise.

Answer: We have revised the practical implications according to the findings of our study.

Reviewer #2:

The manuscript entitled “Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study” compared the motor competence of overweight/obese preschoolers with eutrophic peers. Overall, the manuscript is well written and it approaches an important topic regarding child health. However, there are some issues in this work which should be better addressed by the authors. Both general and specific comments are provided as per below.

We thank the reviewer for the comments and suggestions; they helped improve the quality of our manuscript further.

General comments

Literature provides extensive evidence about the relationship between motor competence and weight status across childhood, yet the background provided by the authors is little informative. As such, it is not clear what is already known about the relationship between body fat and motor competence in preschool children. In addition, the authors argued that “the strength of the present study is the consideration of multiple factors that influence child development” (page 4). However, it is not clear the rationale for considering these multiple factors (i.e. PA, sex, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment) as potential confounders. In addition, it does not seem appropriate to consider “factors that influence child development” in a cross-sectional study.

Also, this cross-sectional study has a small sample size, especially when considering the multiple factors/variables inserted in the regression analysis.

Answer: Suggestion accepted! Because of the lack of studies with preschoolers, we adjusted the entire introduction session to bring theoretical references, providing the basis for understanding how far the literature has advanced the relationship between motor competence and body fat in children. We emphasize that we were careful to pair preschool children in both groups considering the variables influencing child development and could lead to interpretation bias in the primary variables [see the previous study of our team including infants up to 2 years of age (Camargos et al., 2016)]. Of note, we calculated our sample size based on a pilot study with five preschoolers in each group, totaling ten subjects. For sample size calculation, we used the Standard Score Locomotor of the TGMD2 and found an effect size of 0.94 using a minimum difference of 2.70 between the groups, with a standard deviation (SD) of 3.50. (G1=20.1, SD ±4.30 and G2 17.4, SD± 2.70). In addition, we considered a power of 90%, and an alpha error of 5%, being 20 participants required for each group, totaling 40 subjects. For the present study, 48 preschoolers from the database were eligible to participate in the study. Finally, only variables with p<0.2 were included in the multiple linear regression model analysis (stepwise).

Specific comments

Introduction

- Overall, I would suggest to provide a focused background considering the relationship between weight status and motor competence across childhood. This seems the main focus of this study and as such it should be better presented in the Introduction.

Answer: Suggestion accepted! We have provided a specific background considering the relationship between weight status and motor competence across childhood (see lines 44-50, 64-78).

- The state of knowledge about the relationship between weight status and motor competence is missing. Please, provide a more detailed background and explain the ‘why’ we should consider “PA, sex, age, socioeconomic status, maternal education, quality of the home environment and quality of the school environment” as potential confounders.

Answer: Suggestion accepted! Introduction session (lines 64-78).

Methods

“For sample calculation, a power of 90%, and an alpha error of 5% were considered, with 20 participants thus being required for each group, totaling 40 subjects.” (page 5, 2nd paragraph).

And the effect size? Did you calculate the sample size considering the number of total predictors and the effect size?

Answer: Yes! We calculated our sample size considering the number of total predictors and calculated the effect size according to a pilot study with five preschoolers in each group, totaling ten subjects. For sample size calculation, we used the Standard Score Locomotor of the TGMD2 and found an effect size of 0.94 using a minimum difference of 2.70 between the groups, with a standard deviation (SD) of 3.50. (G1=20.1, SD ±4.30 and G2 17.4, SD± 2.70). In addition, we considered a power of 90%, and an alpha error of 5%, being 20 participants required for each group, totaling 40 subjects. For the present study, 48 preschoolers from the database were eligible to participate in the study.

See below the Print Screen of our sample size calculation.

Results

In the Table 3, there two regression models (i.e. pre- post adjustment). Please, explain this analysis in the Methods section.

Answer: To clarify, we have inserted table 4 (multiple linear regression) including the statistical model. Moreover, we have inserted in additional information in Materials and methods

…simple linear regression model between independent variables and the dependent variable LP. Variables with p<0.2 became part of the multiple linear regression model (stepwise).

Discussion

I think the Discussion should be reassessed by the authors considering the previous comments.

Answer: We have revised the discussion session considering the previous comments.

Submitted filename: Response to Reviewers.docx

Click here for additional data file.

17 Jan 2022

31 Jan 2022

Ref: PONE-D-21-16031

Title: Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study

PLOS ONE

Dear Daniel V. Chagas

Academic Editor

PLOS ONE

We appreciate the reviewer’s comments. They were important to improve the quality of our manuscript. See below the point-to-point answers.

PONE-D-21-16031

1) Overall, the manuscript was amended addressing all issues raised by reviewers, including my comments as reviewer in the first round of revision. However, I would like to suggest some papers to be considered in the manuscript, especially in the Introduction and Discussion. These articles are: Hall et al. 2018 (doi:10.3390/jfmk3040057); Wood et al. 2022 (doi: 10.1089/chi.2021.0026); Henrique et al. 2019 (doi.org/10.1002/ajhb.23364)

A) Hall et al. 2018 (doi:10.3390/jfmk3040057

Answer: We appreciate the suggestion. We inserted the reference in the introduction (line 60) “healthy behaviors that may influence physical activity (PA) practices throughout life [10, 11]”.

B) Wood et al. 2022 (doi: 10.1089/chi.2021.0026)

Answer: We appreciate the suggestion. We inserted the reference in the introduction (see lines 67-68: “Although previous work has shown that fat mass was not related to any motor skill measure [13]” and lines 322-323) “Although previous work has shown that fat mass was not related to any motor skill measure [13]”.

C) Henrique et al. 2019 (doi.org/10.1002/ajhb.23364)

We appreciate the suggestion. We inserted the reference in the introduction (see line 69: including a work with Brazilian preschoolers from the Northeast region of Brazil [15]), and in the discussion (see lines 329-330: In this sense, we emphasize that this relationship can be bidirectional from a preschool age [15]). Of note, the suggested article was already listed in the references (see reference 15).

Thank you for contacting us and we are at your disposal for any questions you may have.

Sincerely,

Juliana Nobre, PhD

Universidade Federal dos Vales do Jequitinhonha e Mucuri, Brazil

Submitted filename: Response to reviews.docx

Click here for additional data file.

7 Feb 2022

Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study

PONE-D-21-16031R2

Dear Juliana Nobre,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Daniel V. Chagas

Guest Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

15 Feb 2022

PONE-D-21-16031R2

Is body fat mass associated with worse gross motor skills in preschoolers? An exploratory study

Dear Dr. Nobre:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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