Objectively Measured Physical Activity Patterns in Children With Overweight and (Morbid) Obesity Across Different Weight Categories, Age Groups and Gender; Baseline Data of a Multidisciplinary Tailored Intervention Program

Background Reduced physical activity (PA) is associated with childhood obesity and is a target for intervention. This study aimed to assess objectively measured PA patterns in Dutch children across weight categories, age groups and gender at the start of a lifestyle intervention. Methods 202 children with overweight and (morbid) obesity (55% + ± referred to the Centre for Overweight Adolescents and Children’s Healthcare (COACH, Maastricht UMC+) were included. Children were categorized as overweight, obese or morbidly obese according to their BMI z-score. PA was measured with the GT3X Actigraph accelerometer. Results PA levels in children with morbid obesity were higher compared to children with obesity, also after correction for age and gender (corrected difference (B) 118 counts per minute (cpm), p = .006). Sedentary behaviour (SB) was lower in children with morbid obesity compared to children with obesity (B -51 min/day, p = .018). Girls performed signicantly less moderate to vigorous PA than boys (B -11 min/day, p < .001) and with increasing age, children performed less PA (B -46 cpm, p < .001) and SB increased (B 18 min/day, p < .001). Conclusion Weight category morbid obesity, lower age and male gender were positively associated with PA and negatively with SB. These ndings highlight the need for tailored PA promotion.

Alarmingly, morbid obesity is the fastest growing subcategory of childhood obesity also in the Netherlands 2,3 . Obesity in children has serious adverse cardiovascular and metabolic consequences and has been shown to track into adulthood. Therefore, it is of great importance to treat obesity in its earliest stage [4][5][6] .
Reduced physical activity (PA) combined with increased sedentary behaviour (SB) may play an important role in childhood overweight and obesity development 7 . The World Health Organization, as well as the Dutch government, recommend that children and adolescents should spend a minimum of 60 minutes in moderate to vigorous PA (MVPA) each day, more vigorous intensity activities should be included when possible and SB should be minimalized 8 . Subjectively measured data showed that 45% of Dutch children (4)(5)(6)(7)(8)(9)(10)(11) year-old) and 69% of adolescents (aged 12-18 years) do not meet these public health guidelines 1 . It is expected that the prevalence of children and adolescents with obesity meeting the activity guidelines is lower, since research has shown that children with overweight and obesity are less frequently physically active compared to their normal-weight peers 9 .
PA promotion plays a central role in the treatment of children with overweight and (morbid) obesity. Tailored interventions are re ned and customized to an individual's situation and needs. To develop such tailored interventions, insight in differences in PA patterns between subgroups is necessary. So far, little is known about the differences in PA across the weight categories overweight, obesity, and morbid obesity. A cross-sectional study that evaluated self-reported PA showed that children with overweight/obesity performed on average (± SD) 69 ± 53 min/day MVPA and morbid obese children performed 51 ± 42 min/day MVPA 10 . Since subjective evaluation of PA often overestimates PA, objective measurements using accelerometry are more accurate to determine the intensity and amount of PA 11 . Andersen et al. (2017) performed objective measurements with GT3X accelerometry and showed that children with obesity spent 39 minutes of MVPA per day 12 . However, neither weight categories nor gender or age categories were distinguished.
Age and gender are factors that need to be taken into account when investigating PA between weight categories since previous studies in the general population showed that boys are more physically active than girls and that PA declines in both genders with age 13,14 . Results of studies that included children having overweight and obesity showed similar results 15,16 . According to Jago et al. (2019), levels of MVPA decreased with increasing age starting from the age of 6 years 15 . In addition, differences in MVPA between BMI categories increase over time, i.e. PA decreases with increasing age for children with overweight/obesity 15 . The study of Rancourt et al. (2018) showed that boys having overweight/obesity were more physically active compared to girls with overweight/obesity 16 . In summary, various studies investigated PA levels in children with overweight and obesity, however, they did not investigate PA levels for the morbid obesity category speci cally and did not compare these results with the overweight-and obese category. In addition, it has been suggested that age and gender differences also in uence PA levels. Therefore, the current study aimed to assess objectively measured PA patterns across different weight categories, age groups, and gender in Dutch children with overweight and (morbid) obesity. It is hypothesized that there are differences in PA between weight categories. Further is is hypothesized that the variables age and gender in uence the amount of PA; i.e. boys perform more PA compared to girls and that with increasing age children perform less PA. Insight in PA in different subcategories might help to improve tailored childhood obesity interventions.

Setting and subjects
This study was designed and conducted within the setting of the Centre for Overweight Adolescent and Children's Health Care (COACH) at the Maastricht University Medical Centre (Maastricht, the Netherlands). Children were referred to COACH by the Child Health Clinics and general practitioners. Within COACH, the children and their families receive a personalized ambulatory and interdisciplinary care program. All children and their families were offered individual guidance with focus on lifestyle changes as published previously 17 . The present study involves a cross-sectional analysis of PA data at intervention onset. Periods of recruitment were from November 2013 until September 2015, and from January 2017 until April 2019. The ActiGraph GT3X (Actigraph, Corp, USA) accelerometer was provided to a random group of 286 participants (89% of the total population), aged 4-18 years. Children suffering from any musculoskeletal condition that would prevent the subject from performing PA or children that were wheelchair dependent did not receive an accelerometer. Figure 1 provides an overview of the inclusion procedure of the study. Subsequently written informed consent was obtained from children aged > 12 years and their parents. The study is registered at ClinicalTrial.gov (registration number: NCT02091544).

Measurements Accelerometry
The Actigraph GT3X is a triaxial accelerometer. The participants were asked to wear the accelerometer attached via a waistband on the right hip bone for seven consecutive days during waking hours, except during water activities (e.g. showering, swimming) and contact sports (e.g. judo). Accelerometry data were downloaded using 10 s epochs using Actilife software (Actigraph, Corp, USA). Valid wear time was de ned as a minimum of 4 days, consisting of at least 480 minutes per day of recording, including one weekend day. Derived data was expressed as mean counts per minute (cpm).

Anthropometrics
Anthropometric data were collected in the morning after an overnight fast, barefoot and wearing only underwear. Body mass was determined using digital scales (Seca, Chino, CA, USA) to the nearest 0.1 kg and height was measured to the nearest 0.1 cm using a digital stadiometer (De Grood Metaaltechniek, Nijmegen, The Netherlands). BMI (weight [kg] / height [m] 2 ) was calculated and BMI z-scores were obtained using a growth analyser (Growth Analyzer VE, Rotterdam, The Netherlands), to adjust for age and gender. Children were categorized as overweight, obese or morbidly obese based on International Obesity Task Force (IOTF) criteria 19 , corresponding to the 90th, 99th and 99.8th percentile respectively. Body composition was measured with the BodPod System (Life Measurement Corporation, Inc.), an air displacement plethysmograph that uses the principle of whole-body densitometry. Lohman's equation was used to determine fat mass (FM) and fat free mass (FFM) from measured body density 20 . All anthropometric measurements were performed by trained health care personnel.

Statistical analysis
Differences between groups (IOTF: overweight, obesity, morbid obesity; gender: male, female; age: <12, ≥ 12 years) were assessed using ANOVA or independent-samples t-tests for numerical variables and chi-square tests for categorical variables. Multivariable linear regression analyses were used to evaluate the associations between PA and weight categories, gender, and age. As additional analyses, age was also dichotomized to distinguish primary school children (4-12 y) and secondary school children (≥ 12 y). Assumptions were checked using plots (scatterplots for linearity, P-P-plots and histograms for normality, residual plots for homoscedasticity), where Cook's distance > 1 was used to de ne in uential outliers. As sensitivity analyses, the multivariable linear regression analyses performed were repeated for weekend-and weekdays separately. A p-value ≤ .05 was considered statistically signi cant. All analyses were performed using IBM SPSS Statistics for Windows version 25.0 (IBM Corp., Armonk, NY, USA).

Results
A total of 202 children were eligible for this study, of which 29% presented with overweight, 46% with obesity and 25% with morbid obesity ( Table 1). The wear-time of the accelerometer was on average (± SD) 851 ± 132 min/day. There were no signi cant differences in wear-time between the different weight categories. Children spent on average 589 ± 142 min/day in SB which correspondents to 69% of the day (based on wear-time). In addition, children spent on average 221 ± 63 min/day of LPA per day and 41 ± 19 min/day of MVPA. Sixteen percent (n = 32) of the children reached the PA guideline of a minimum 60 minutes of MVPA per day. Physical activity differences between weight categories, age and gender Children with morbid obesity were signi cantly more physically active (851 ± 357 cpm vs 715 ± 263 cpm, p = .009) and less sedentary (547 ± 154 min/day vs 606 ± 138 min/day p = .018) compared to children with obesity (Table 1). Table 2 shows that after correcting for age and gender, children with morbid obesity performed more total PA (cpm) (corrected difference (B) = 188, p = .006) and less SB (B=-51 p = .024) compared to children with obesity. Boys were signi cantly more physically active (861 ± 330 cpm versus 698 ± 253 cpm, p = < .001) and performed more MVPA (47 ± 20 versus 36 ± 16 min/day, p = < .001) compared to girls. In addition, for each year increase of age, PA decreases on average with 46 cpm (p = < .001) and SB increases with 18 min/day (p = < .001). As additional analyses, we distinguished primary school children (4-12 y) and secondary school children (≥ 12 y). Primary school children were more physically active compared to secondary school children (910 ± 300 cpm versus 634 ± 227 cpm, p < .001). Physical activity behavior on week-and weekend day Table 3 shows that after correcting for age and gender, children with morbid obesity perform more total PA (cpm) during weekdays (B = 122, p = .005) as well as during weekend days (B = 130, p = .030) compared to children with obesity. In addition, for each year increase in age PA decreases both on weekdays (B=-45, p = < .001) and weekend days (B=-50, p = < .001).

Discussion
The current study evaluated objectively measured PA patterns of children with overweight, obesity and morbid obesity across different weight categories, age groups and gender, at the start of a lifestyle intervention program. On average, participants spent 589 min/day in SB and 41 min/day in MVPA. Sixteen percent of the children met the PA recommendation of minimum 60 min/day MVPA. Children with morbid obesity performed in total more PA (cpm) than children with obesity. In addition, children with morbid obesity showed less SB and more LPA. Also during weekend days, total PA was higher for children with morbid obesity compared to children with obesity. When PA intensities are expressed as percentages of wear-time, the observed differences remain.
Previous studies that evaluated associations between PA and weight categories showed contradictory results. Page et al. (2005) and Cooper et al. (2000) showed that children with obesity were less physically active compared to children with normal weight 9,21 . Though Gomes et al.
(2014) did not show any association between SB and BMI in children with normal weight, overweight, and obesity 22 . It should be noted that these studies used subjective measures of PA.
Differences in objectively measured PA between weight categories, age groups, and gender in the current study can be explained in various ways. Firstly, the development of overweight or obesity is multifactorial and complex. Not only PA, but also nutrition, metabolic, environmental, psychosocial, and cultural factors are considered to play a central role in obesity development and maintenance. According to Nemet et al.
(2010) food consumption increased after moderate intensity PA in children with overweight. However, food intake decreased after moderate intensity PA in children with normal weight 23 . Based on these ndings, it could be suggested that children with morbid obesity may compensate PA with more calorie intake compared to children with obesity. Another possible explanation may be selection bias and motivational factors as children in this study were referred by the youth and healthcare division. Participants, especially those with morbid obesity, could be more aware of the relevance of PA or showed socially desirable behaviour, which may result in higher motivation to be physically active at the moment of study enrollment. Furthermore, despite the fact that accelerometers are frequently used to measure objective PA behaviour, the effect of adiposity on the accuracy of PA measurements remains unclear. However, there were no signi cant differences in activity counts among weight categories for the Actigraph accelerometer 24 . Therefore, it is expected that the results of the present study between the different weight categories are accurate.
In agreement with the ndings of the present study, previous studies also suggest that in general, boys are more physically active compared to girls and PA levels have been shown to increase with age, up to an age of 10-11 years old, and then decrease at > 11 years when children head into puberty 25,26 . According to the ndings of the present study, boys were more physically active compared to girls and activity counts decreased with age. Speci cally, primary school-aged children (< 12 years) showed higher total PA compared to secondary school-aged children (≥ 12 years). The higher level of total PA in boys could be explained by a higher intrinsic motivation and more experience of enjoyment during PA compared to girls 27 . This knowledge needs to be taken into account in order to stimulate and improve PA, especially amongst girls.
Additionally, the negative association between PA and age highlights the importance of early PA promotion since the presence of comorbidities is already evident in primary school children with obesity 28 .
Limitations were the cross-sectional design of the study and the absence of a power-calculation. The results of the current study highlights the importance of the development of tailored intervention strategies based on these ndings. In addition, the results of the current study provide new insights for medical specialists, health professionals but also sport coaches/ physical educational teachers, who can stimulate and motivate children to perform PA.

Conclusion
In conclusion, this cross-sectional study showed that children with overweight and (morbid) obesity spent on average 41 min in MVPA per day and 16% of the children reached the PA guidelines of 60 minutes MVPA per day. Weight category, age and gender are associated with PA since children with morbid obesity performed more total PA and less SB compared to children with obesity, PA levels were higher for boys compared to girls and PA levels decreased with ageing. These ndings highlight the need for tailored PA promotion and reducing SB. Follow up data of children participating in the COACH program need to examine the effect of the lifestyle intervention on PA across overweight categories including age and gender. Ethics approval and consent to participate

List Of Abbreviations
The current study was conducted according to the Declaration of Helsinki and approved by the medical ethical committee of the azM and Maastricht University (METC azM/UM). Subsequently written informed consent was obtained from children aged > 12 years and their parents.

Consent for publication
Not applicable.

Availability of data and materials
All data generated or analysed during this study are included in this published article.

Competing interests
The authors declare that they have no competing interests.