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Article

Benefits in Cardiac Function from a Remote Exercise Program in Children with Obesity

by
Savina Mannarino
1,†,
Sara Santacesaria
1,†,
Irene Raso
1,†,
Massimo Garbin
1,
Andreana Pipolo
1,
Silvia Ghiglia
1,
Gabriele Tarallo
1,
Annalisa De Silvestri
2,
Matteo Vandoni
3,
Daniela Lucini
4,5,
Vittoria Carnevale Pellino
3,6,
Giuseppina Bernardelli
5,7,
Alessandro Gatti
3,
Virginia Rossi
8,
Valeria Calcaterra
8,9,* and
Gianvincenzo Zuccotti
8,10
1
Pediatric Cardiology Unit, Pediatric Department, Buzzi Children’s Hospital, 20154 Milan, Italy
2
Biometry & Clinical Epidemiology, Scientific Direction, Fondazione IRCCS Policlinico San Matteo, 27100 Pavia, Italy
3
Laboratory of Adapted Motor Activity (LAMA), Department of Public Health, Experimental Medicine and Forensic Science, University of Pavia, 27100 Pavia, Italy
4
BIOMETRA Department, University of Milan, 20129 Milan, Italy
5
Exercise Medicine Unit, Istituto Auxologico Italiano, IRCCS, 20135 Milan, Italy
6
Department of Industrial Engineering, University of Rome Tor Vergata, 00133 Rome, Italy
7
DISCCO Department, University of Milan, 20122 Milan, Italy
8
Pediatric Unit, Pediatric Department, Buzzi Children’s Hospital, 20154 Milan, Italy
9
Department of Internal Medicine, University of Pavia, 27100 Pavia, Italy
10
Department of Biomedical and Clinical Science, University of Milano, 20157 Milan, Italy
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Int. J. Environ. Res. Public Health 2023, 20(2), 1544; https://doi.org/10.3390/ijerph20021544
Submission received: 15 December 2022 / Revised: 11 January 2023 / Accepted: 12 January 2023 / Published: 14 January 2023

Abstract

:
Physical activity (PA) is a crucial factor in preventing and treating obesity and related complications. In this one-arm pre–post longitudinal prospective study, we evaluated the effects of a 12-week online supervised training program on cardiac morphology, function and blood pressure (BP) in children with obesity. The training program consisted of three sessions per week, each lasting 60 min. Advanced echocardiographic imaging (tissue Doppler and longitudinal strain analysis) was used to detect subclinical changes in heart function. Categorical variables were described as counts and percentages; quantitative variables as the mean and standard deviation (SD) as they were normally distributed (Shapiro–Wilks test). Pre–post comparisons were made with a paired t-test. A total of 27/38 (71%) enrolled patients (18M/9F, 11 ± 2 years) completed the training protocol and were considered in the analysis. At baseline, no hypertensive patient was noted; all echocardiographic variables were within the normal range. After training, we observed a significant reduction in BP parameters, including systolic BP values and Z-score, diastolic BP values, centiles and Z-score, and mean arterial pressure (all p < 0.05). Significant variations in echocardiographic interventricular septum (IVSd) thickness (p = 0.011), IVSd Z-score (p = 0.001), left ventricular (LV) end-diastolic diameter (p = 0.045), LV posterior wall thickness Z-score (p = 0.017), and LV global longitudinal strain (p = 0.016) were detected. No differences in LV diastolic function and right ventricular strain were noted. PA plays a decisive role in improving BP control and has benefits on left ventricle systolic function, representing a strategic approach to limit CV risk. Online exercise could be an excellent method of training in children with obesity.

1. Introduction

The increasing incidence of obesity has become a significant public health concern [1]. The World Health Organization (WHO) estimated that more than 39 million children under the age of 5 years old are overweight or obese [2]. This epidemy is widespread due to the interactions between multiple factors, including genetic, biological, developmental, behavioral and cultural issues [3].
Obesity in childhood affects multiple organ systems in an adverse manner, causing insulin resistance, dyslipidemia, type 2 diabetes mellitus (T2DM), metabolic syndrome, non-alcoholic fatty liver disease (NAFLD), excess stress on the musculoskeletal system [4,5,6], pulmonary disorders (obstructive sleep apnea, asthma and chronic obstructive pulmonary disease) related to direct mechanical changes due to fat deposition, decreased pulmonary volume, restricted diaphragmatic mobility and rib movement [7,8], pro-inflammatory state, and psychological and social problems [9].
Furthermore, obesity has a great impact on the cardiovascular system [10,11]; the body mass index (BMI) in children and adolescents has been shown to have a positive correlation with the risk of heart disease in adults, suggesting that cardiovascular damage may begin during childhood [12]. The excessive adiposity increases the metabolic request of the body, resulting in an increased blood volume and preload of the heart [13]. Moreover, the increased peripheral vasoconstriction and renal tubular sodium reabsorption, together with the augmented sympathetic activity and the overactivation of the renin–angiotensin system, contribute to vascular alterations such as increased arterial stiffness and resistance [14]. Those alterations lead to an augmented afterload of the heart, to both concentric and eccentric hypertrophy and to the obesity-related hypertension with arterial wall damage [15]. Furthermore, the cardiac structure can be modified by being overweight: research in children with obesity demonstrated a positive relationship between BMI and cardiac dimensions and an increased left ventricular (LV) mass compared with normal weight children [16,17,18]. Altered morphology has been associated with impaired cardiac function. Diastolic dysfunction has been reported in children with obesity and strain and strain rate analyses have shown contractile abnormalities even within those with a normal LV ejection fraction [19,20]. A reduction in longitudinal strain is a sensitive measure and a predictor of cardiovascular disease and mortality [21].
Despite how widespread this disease is, interventions for the prevention and management of obesity in children are still not well defined and difficult to assess [22] Physical activity (PA) is a crucial factor in the fight against overweight and the literature agrees on advocating exercise as among the most useful tools for both the prevention and treatment of obesity and related complications [23]. Among PA benefits, there are the increase in muscular strength, the improvement in endothelial function, the reduction in insulin resistance and lipid profile, the reverse of cardiovascular impairment and the reduction in blood pressure [24,25,26]. Moreover, exercise was demonstrated to improve the cardiac function measured as global longitudinal strain in adults and children with cardiovascular disease [21,27]. However, PA can also be difficult to practice for children with obesity due to psychological problems related to body shame and social pressure; but no studies have been made to test the feasibility of a program of online exercise.
The aim of this study was to evaluate the effects of a program of remote PA on echocardiographic and blood pressure (BP) parameters in children with obesity. The use of advanced echocardiographic imaging, such as tissue Doppler and longitudinal strain analysis, has been made to detect subclinical changes in heart function. The hypothesis is that online exercise could improve cardiac function and arterial pressure, regardless of weight loss. PA training in remote modalities may also represent a useful tool to prevent early cardiovascular risk [21,23,28].

2. Material and Methods

2.1. Patients

This is a one-arm pre–post longitudinal prospective study performed at the Pediatric Department of the Children’s Hospital Vittore Buzzi of Milan with the collaboration of Laboratory of Adapted Motor Activity (LAMA), University of Pavia, Italy. A total of thirty-eight children with obesity, referred to our pediatric unit for obesity by their primary care pediatric consultant, were consecutively enrolled (March 2021–November 2021) in this study. Obesity was defined as a BMI z-score ≥ 2 according to the World Health Organization [2]. Patients suffering from chronic illnesses, taking medications, with contraindications to the practice of PA or whose obesity was due to a secondary condition were excluded. Twenty-seven patients accomplished the training protocol and completed cardiologic follow up. To better understand the exclusive effect of PA on blood pressure (BP) and cardiac function, no personalized calorie restriction regimen was provided during the observation period in our study.

2.2. Methods

2.2.1. Auxological Evaluation

In all the participants, height, weight, puberal stage, BMI, BMI z-score, waist circumference (WC), and waist-to-height ratio (WHtR) were measured as previously described [29]. Briefly, weight was measured using a scale platform (Seca, Hamburg, Germany) with children not wearing shoes and in light clothing, standing upright, hands at their sides, and looking straight ahead. Height was measured using a Harpenden stadiometer (Holtain Ltd., Cross-well, UK) [29]. BMI was calculated as body weight (kilograms) divided by height (meters squared) and converted into BMI z scores using WHO reference values [30]. WC was measured in the horizontal plane midway between the lowest ribs and the iliac crest, using a flexible inch tape [29]. Waist to height ratio (WHtR) was calculated according to Maffeis [31]. Puberal stages were considered according to Tanner and classified as prepuberal stage 1 = Tanner 1; middle puberty stage 2 = Tanner 2–3; late puberty stage 3 = Tanner 4–5 [29].

2.2.2. Cardiologic Assessment

Cardiological evaluation with BP and echocardiography was performed before (T0) and within one week after the completion of the physical fitness protocol (T1). All children underwent standard and advanced transthoracic echocardiography (TTE), recorded with Vivid S5 GE Healthcare by a single pediatric cardiologist (M.G.) and validated by a second cardiologist (S.S). Standard echocardiographic measurements were made according to the American Society of Echocardiography Guidelines [32], including M-mode of the left ventricle (LV), diastolic LV function with mitral inflow peak velocities and tissue doppler images (TDI) of septal and lateral annular peaks and LV mass indexed for height [33]. Z-score indexed for body surface area were calculated according to the Detroit z-score [34]. The advanced TTE analysis included measures of myocardial deformation. Analysis was performed offline with independent software (TOMTEC Imaging Systems GmbH). Global longitudinal strain (GLS) was calculated as the average of the peak systolic longitudinal strain from all LV segments and for the RV function, the peak longitudinal strain of the free wall (RVFWLS) was measured from a 4-chamber image. According to published vendor normal range, we considered age-dependent normal values with a 95% confidence interval: 2–9 years old −21.7% (95% CI, −23.0% to −20.5%), 10–13 years old from −20% (95% CI, −20.8% to −19.1%) and 14–21 years old −19.9% (95%CI, −20.6% to −19.2%) [35]. If the values were within the normal range, a change in at least 10% from baseline in LVGLS was considered a significant variation. Peak global left atrial reservoir strain (LAS) was recorded from the 4-chamber view, as a diastolic function parameter.
BP was detected using multiple office blood pressure measurement (MOBP): systolic and diastolic values were the result of the arithmetic mean of ten successive measurements. Percentiles and z-scores [36] of the collected values were identified to investigate any variation after the intervention.

2.2.3. Physical Fitness (PF) Tests

To evaluate PF in children, we used common field test batteries. Prior to and after the training protocol period, we assessed different domains of PF: cardiovascular fitness through the 6 min walking test performed in accordance with international guidelines [37,38], lower-limb power and strength through the standing broad jump [39,40] and speed-agility assessed through the 5 × 10 sprint test [41]. All procedures are described elsewhere [37,40,41,42,43,44]. During the test and training execution, we assessed the children’s effort with the Children’s Effort Rating Table (CERT) [45] to ensure the safety of the protocol. All the PF measurements were taken by two sport specialists after a two-week period of familiarization.

2.2.4. Training Protocol

Children performed the training protocol for 12 weeks with three 60 min online sessions (on Mondays, Wednesdays and Fridays) per week, totaling 36 sessions that were supervised by two expert trainers. According to the literature, a 12-week protocol is sufficient to improve both physical fitness and health outcomes in children with obesity, reducing the risk of exercise program abandonment [46,47,48,49]. The training program was implemented from April to June 2021 and from September to December 2021. The exercise sessions were always performed from 5 PM to 6 PM, after school. Each session was streamed using the Zoom® platform in real time, allowing live interaction among instructors and children. Moreover, three days per week, participants had to exercise individually using a YouTube channel (“LAMA Junior”) implemented with training video routines by the sport specialists. All the training sessions were structured with a 5–10 min warm-up, 20 min of aerobic interval training, 20 min of a strength circuit, and 5–10 min of cool-down or stretching [44]. All the routines were proposed through playful and recreative activities and did not require any specific equipment. An example of the exercises proposed are shown in a previous study of Vandoni et al. (2022) [44]. To understand the intensity of the training session, the heart rate during the session was monitored with an activity tracker (Fitbit Charge 2©, Fitbit Inc., San Francisco, CA, USA), to stay between 60 and 80% of their maximum heart rate to reach an intensity classifiable from moderate to vigorous and registered by the trainers after 30 min from the beginning of the sessions. Moreover, before each exercise, trainers reminded children to maintain a safety effort based (low–moderate intensity) on a CERT scale value, as described elsewhere [50].

2.3. Statistical Analysis

Categorical variables were described as counts and percentages; quantitative variables as the mean and standard deviation (SD) as they were normally distributed (Shapiro–Wilks test). Pre–post comparisons were made with a paired t-test. All analyses are performed with Stata v17.0 (StataCorp USA). Power consideration: with 27 subjects, it will be possible to achieve a power >90% to find a significant (p < 0.05) mean pre–post difference when SD is 1.5-fold greater than mean difference.

3. Results

In Table 1 are reported the baseline characteristics of the 27 patients with obesity (18 males, 9 females, aged 11 ± 2 years, range 8–15) who completed the training protocol (adherence to the exercise program of 90%).
All patients underwent a cardiac evaluation at baseline and within one week after the end of the PA program (T1).
An improvement was recorded between baseline and after the exercise program in WHtR without reaching statistical significance (p = 0.06); no significant differences were noted in BMI z-score (p = 0.38) and WC (p = 0.52). Puberal stage remained stable in all patients, except in two in which there was a progression from prepuberty to middle puberty (p = 0.19).
In our population, at baseline, no patient was hypertensive but 6/27 (22.2%) had high–normal systolic pressure before intervention (Z-score between 2 and 3) and 4/6 (66.7%) improved their Z-score to <2.
Table 2 presents variations in BP from baseline (T0) to after training control (T1). A statistically significant reduction in all the BP parameters was observed after intervention: systolic BP values (p= 0.05) and systolic BP Z-score (p = 0.027), diastolic BP values (p= 0.001), diastolic centiles (p <0.063) and diastolic BP Z-score (p <0.001) and mean arterial pressure (MAP) (p= 0.002).
Concerning the echocardiographic evaluation, at baseline, all the measured variables were within the range of normality for body surface area and age. We recorded only 6 subjects (22.2%) with a mildly increased left ventricular end-diastolic diameter (LVEDD) with a LVEDD z-score between 2 and 3. Both left ventricular diastolic and systolic function were normal at baseline and remained normal at the follow-up. Table 3 depicts variations in echocardiographic parameters at baseline and after training (T1).
A statistically significant variation was evident for interventricular septum thickness (IVSd) (p = 0.011) and IVSd z-score (p-value 0.001), for the left ventricular end-diastolic diameter (p = 0.045) and the left ventricular posterior wall thickness z-score (p-value 0.017). LV mass indexed for height values showed no significant differences between T0 and T1 (p = 0.39).
The advanced evaluation did not show differences in LV diastolic function and right ventricular strain. The left ventricular global longitudinal strain (LVGLS) was normal at baseline but improved significantly after the completion of the PA program (p-value 0.016). In 11/27 patients (40.7%), a 10% LVGLS improvement was noted after training compared to baseline (range 10–22%).

4. Discussion

2Childhood obesity is a multisystem disease that leads to several comorbidities, cardiovascular diseases, hypertension, T2DM, NAFLD, hyperlipidemia and other conditions associated with chronic inflammation, which cause disability and shorten the life span [51]. Even if the effects of the increased cardiometabolic risk develop progressively, the combination of multiple risk factors certainly results in more severe consequences. Diet and PA combined is a useful non-pharmacological strategic intervention to reduce obesity-related complications. PA shows positive effects in reducing weight, improving insulin sensitivity, alleviating plasma dyslipidemia, normalizing BP, decreasing blood viscosity, reducing oxidative stress, improving leptin sensitivity and consequently protecting the heart and vessels [52,53,54] to reduce cardiovascular risk from childhood to adulthood [23,55].
This study was performed to evaluate the cardiovascular effects of remote PA in children with overweight and obesity, without providing a dietary regimen and therefore regardless of weight loss. Our study shows satisfactory participation in the project, with 71% of the children who completed the training program. Concerning the effect of exercise on BP, our analysis showed a significant improvement in all systolic, diastolic and MAP values of both absolute and BP z-score. Although there were no patients with hypertension in our population at baseline, 22% of them had high–normal systolic pressure before intervention, and 66.6% of them improved their Z-score. At the echocardiographic evaluation, normal chamber morphology and cardiac function at baseline was noted in all patients, indicating that obesity-related cardiac dysfunction was still not clinically evident in our population. Nevertheless, the echocardiographic assessment also showed a statistically significant reduction in IVSd and PWd thickness when considering concomitant child growth. In contrast, statistically significant increase in the absolute value of the LVEDD did not correspond to a significant Z-score increase, demonstrating that this parameter is likely to be dependent on patient growth. No significant changes occurred in parameters related to diastolic dysfunction and all patients had normal baseline global longitudinal strain, which further improved at T1; 41% of subjects showed a significant improvement in the LVGLS after the training program, considering a 10% change from baseline in LVGLS a significant variation [21,56]
A positive effect in multiple measures of muscular and cardiorespiratory fitness in children with overweight and obesity [57] is proven in team sports such as football [58] and recreational activities as well as active video games (“exergames”) [59]. However, less is known about the effect of the remote training program adapted to children with obesity. In our study, the high adherence to the PA program could be supported by the possibility to perform PA online, taking advantage of videos, exergames and personal training. Moreover, remote training offers numerous advantages in terms of feasibility, personal adaptation, cost effectiveness and psychological aspects; in fact, the children are in a familiar environment and freed from social pressures. Furthermore, PA increases parasympathetic activity, certainly influencing the autonomic system, arterial stiffness and endothelial function [11] in healthy subjects and patients with obesity. Our data confirm the positive effect of exercise on BP even when it is not conducted at high intensity and for a relatively short time. Moreover, BP changes affect left ventricular wall thickness. In our patients, the reduction in IVSd and PWd thickness after PA could be related to improvement in BP; however, no significant changes in LV cardiac mass were evident after the intervention. A possible explanation could be that the majority of patients had normal BP values at baseline, and thus did not show latent signs of cardiac mass modification in such a short time; further evaluation in a large population is needed for a better understanding. The absence of significant changes in diastolic function is probably due to the age of our population because impairment occurs later and requires a more severe cardiovascular compromise to manifest. On the other hand, the improvement in LV strain may suggest that PA and BP optimization bring functional advantage to LV, even between parameters in the normal range. It is hypothesized that another important role of physical activity on cardiac function and BP may depend on the effects of exercise on the autonomic nervous system. However, this hypothesis could not be analyzed in our study due to the low sample size.
It is well known that obesity can cause hypertension and that obesity and hypertension together can cause increased metabolic demand and cardiac remodeling, leading to high end-diastolic pressure and to diastolic dysfunction [60]. However, the effects of obesity on LV systolic function are less known with several studies which have reported a normal or even a supranormal ejection fraction in adult populations with obesity [61]. More advanced measurements, such as ventricular strain analysis, also showed subclinical myocardial dysfunction in those with a normal ejection fraction [19,20]. Our study results are in line with a recent metanalysis that Murray J. et al. [21] conducted on a large adult population: in that study, a significant change in LV strain was found after the physical exercise program lasting at least two weeks. Interestingly, they found a moderate effect on LVGLS only in the CV risk population and they found no effect in the healthy subgroup, and the effect of PA was independent to exercise intervention length. In the literature, data about the effect of PA on cardiac function in children are few and sometimes discordant. Obert P et al. [62] demonstrated that after a 13-week running program, cardiac dimension increased, and wall thickness decreased. In an old study, Hayashi et al. [63] reported a significant change in LV mass and dimension after 1 year of training in children with obesity. Those finding are in line with our data. However, another two studies (one in overweight children [27] and another in healthy children [64]) reported increased PWd thickness after training. The first study [27] was conducted among 20 children with obesity after 3 months of a football training intervention vs. a controlled group without a physical activity intervention. They demonstrated a relative reduction in BP in the intervention group compared to the control group, and no modifications in LVGLS [27]. However, Z-scores were not evaluated, and the type of PA is not comparable in the studies. Further research will help to better define the effect of PA on PWd thickness and left ventricle longitudinal myocardial deformation in childhood.
The main limitation of this study is the small number of participants; an increased sample size will be useful to validate these results, offering the possibility to also assess the effect of BP on cardiac function. Moreover, the effect of heart rate variability and autonomic activity could be not excluded; heart rate potentially reflects changes in sympathetic activity and may influence both BP values and cardiac function. Additionally, as adiposity indices, we considered only clinical parameters, which are inaccurate measures of body components; using a tool for the examination of body composition may be useful to evaluate the relationship between changes in fat and/or lean mass and echocardiographic assessment.
The findings of our study confirmed the importance of PA as a key treatment tool for improving health outcomes and preventing and reversing CV modifications in patients with obesity at any age. Online physical exercise is an interesting activity to be proposed for overweight children and could be implemented in schools or included as part of a medical program for the prevention and treatment of obesity.

5. Conclusions

Our study confirms that physical exercise plays a decisive role in improving BP and has positive effects on left ventricle systolic function, measured with advanced techniques. To prevent the progression of obesity from childhood to adulthood as well as the development of CV risks, it is necessary to teach children to exercise regularly. PA increases physical fitness and modifies children’s cardiometabolic risk even after a short period of training. Online exercise could be an excellent method of training for the pediatric population: it is appreciated by children and adolescents and could be more manageable for families.

Author Contributions

Conceptualization, S.M., S.S., I.R., M.G. and V.C.; methodology, S.M., S.S., I.R., M.G., A.P., S.G., G.T., A.D.S., M.V., D.L., V.C.P., G.B., A.G., V.R., V.C. and G.Z.; writing—original draft preparation, S.M., S.S., I.R., M.G., A.P., S.G., G.T., A.D.S., M.V., V.C.P., G.B., A.G., V.R. and V.C.; writing—review and editing, S.M., S.S., I.R., M.G., A.D.S., M.V., D.L., V.C.P., V.C. and G.Z.; supervision, S.M., M.V., D.L., V.C. and G.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially funded by the Italian Ministry of Health.

Institutional Review Board Statement

This study protocol was part of a project on early-risk cardiovascular prevention. It was approved by an Ethical Committee (protocol number 2020/ST/298).

Informed Consent Statement

Parents/guardians gave written informed consent to participate on description of this study; children could withdraw from the program at any moment without consequences.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kelly, T.; Yang, W.; Chen, C.S.; Reynolds, K.; He, J. Global burden of obesity in 2005 and projections to 2030. Int. J. Obes. 2008, 32, 1431–1437. [Google Scholar] [CrossRef] [Green Version]
  2. World Health Organization. Obesity and Overweight. 2021. Available online: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight (accessed on 1 November 2022).
  3. Qasim, A.; Turcotte, M.; de Souza, R.J.; Samaan, M.C.; Champredon, D.; Dushoff, J.; Speakman, J.R.; Meyre, D. On the origin of obesity: Identifying the biological, environmental, and cultural drivers of genetic risk among human populations. Obes. Rev. 2018, 19, 121–149. [Google Scholar] [CrossRef] [PubMed]
  4. Gurnani, M.; Birken, C.; Hamilton, J. Childhood obesity: Causes, consequences, and management. Pediatr. Clin. N. Am. 2015, 62, 821–840. [Google Scholar] [CrossRef]
  5. Sahoo, K.; Sahoo, B.; Choudhury, A.K.; Sofi, N.Y.; Kumar, R.; Bhadoria, A.S. Childhood obesity: Causes and consequences. J. Family Med. Prim. Care 2015, 4, 187–192. [Google Scholar] [CrossRef]
  6. Barnett, T.; Kelly, C.; Young, D.; Perry, C.; Pratt, C.; Edwards, N.; Rao, G.; Vos, M. Sedentary Behaviors in Today’s Youth: Approaches to the Prevention and Management of Childhood Obesity: A Scientific Statement From the American Heart Association. Circulation 2018, 38, e142–e159. [Google Scholar] [CrossRef] [PubMed]
  7. Davidson, W.J.; Mackenzie-Rife, K.A.; Witmans, M.B.; Montgomery, M.D.; Ball, G.D.; Egbogah, S.; Eves, N.D. Obesity negatively impacts lung function in children and adolescents. Pediatr Pulmonol. 2014, 49, 1003–1010. [Google Scholar] [CrossRef] [PubMed]
  8. Mafort, T.T.; Rufino, R.; Costa, C.H.; Lopes, A.J. Obesity: Systemic and pulmonary complications, biochemical abnormalities, and impairment of lung function. Multidiscip. Respir. Med. 2016, 11, 28. [Google Scholar] [CrossRef] [Green Version]
  9. Topçu, S.; Orhon, F.S.; Tayfun, M.; Uçaktürk, S.A.; Demirel, F. Anxiety, depression, and self-esteem levels in obese children: A case-control study. J. Pediatr. Endocrinol. Metabol. 2016, 29, 357–361. [Google Scholar] [CrossRef]
  10. Daniels, S.R. Complications of obesity in children and adolescents. Int. J. Obes. 2009, 33 (Suppl. 1), S60–S65. [Google Scholar] [CrossRef] [Green Version]
  11. Cote, A.T.; Harris, K.C.; Panagiotopoulos, C.; Sandor, G.G.; Devlin, A.M. Childhood obesity and cardiovascular dysfunction. J. Am. Coll Cardiol. 2013, 62, 1309–1319. [Google Scholar] [CrossRef]
  12. Acree, L.S.; Comp, P.C.; Whitsett, T.L.; Montgomery, P.S.; Nickel, K.J.; Fjeldstad, A.S.; Fjeldstad, C.; Gardner, A.W. The influence of obesity on calf blood flow and vascular reactivity in older adults. Dyn. Med. 2007, 6, 4. [Google Scholar] [CrossRef] [Green Version]
  13. Alpert, M.A. Obesity cardiomyopathy: Pathophysiology and evolution of the clinical syndrome. Am. J. Med. Sci. 2001, 321, 225–236. [Google Scholar] [CrossRef]
  14. Lobato, N.S.; Filgueira, F.P.; Akamine, E.H.; Tostes, R.C.; Carvalho, M.H.; Fortes, Z.B. Mechanisms of endothelial dysfunction in obesity-associated hypertension. Braz. J. Med. Biol. Res. 2012, 45, 392–400. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Vasan, R.S. Cardiac function and obesity. Heart 2003, 89, 1127–1129. [Google Scholar] [CrossRef]
  16. Mehta, S.K.; Richards, N.; Lorber, R.; Rosenthal, G.L. Abdominal obesity, waist circumference, body mass index, and echocardiographic measures in children and adolescents. Congenit. Heart Dis. 2009, 4, 338–347. [Google Scholar] [CrossRef]
  17. Ozdemir, O.; Hizli, S.; Abaci, A.; Agladioglu, K.; Aksoy, S. Echocardiographic measurement of epicardial adipose tissue in obese children. Pediatr. Cardiol. 2010, 31, 853–860. [Google Scholar] [CrossRef]
  18. Dhuper, S.; Abdullah, R.A.; Weichbrod, L.; Mahdi, E.; Cohen, H.W. Association of obesity and hypertension with left ventricular geometry and function in children and adolescents. Obesity 2011, 19, 128–133. [Google Scholar] [CrossRef] [PubMed]
  19. Peterson, L.R.; Waggoner, A.D.; Schechtman, K.B.; Meyer, T.; Gropler, R.J.; Barzilai, B.; Dávila-Román, V.G. Alterations in left ventricular structure and function in young healthy obese women: Assessment by echocardiography and tissue Doppler imaging. J. Am. Coll. Cardiol. 2004, 43, 1399–1404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Wong, C.Y.; O’Moore-Sullivan, T.; Leano, R.; Byrne, N.; Beller, E.; Marwick, T.H. Alterations of left ventricular myocardial characteristics associated with obesity. Circulation 2004, 110, 3081–3087. [Google Scholar] [CrossRef] [Green Version]
  21. Murray, J.; Bennett, H.; Bezak, E.; Perry, R.; Boyle, T. The effect of exercise on left ventricular global longitudinal strain. Eur. J. Appl. Physiol. 2022, 12, 1397–1408. [Google Scholar] [CrossRef]
  22. Daniels, S.R.; Jacobson, M.S.; McCrindle, B.W.; Eckel, R.H.; Sanner, B.M. American Heart Association Childhood Obesity Research Summit Report. Circulation 2009, 119, e489–e517. [Google Scholar] [CrossRef] [Green Version]
  23. Calcaterra, V.; Zuccotti, G. Physical Exercise as a Non-Pharmacological Intervention for Attenuating Obesity-Related Complications in Children and Adolescents. Int. J. Environ. Res. Public Health 2022, 19, 5046. [Google Scholar] [CrossRef] [PubMed]
  24. Lee, Y.H.; Song, Y.W.; Kim, H.S.; Lee, S.Y.; Jeong, H.S.; Suh, S.H.; Park, J.K.; Jung, J.W.; Kim, N.S.; Noh, C.I.; et al. The effects of an exercise program on anthropometric, metabolic, and cardiovascular parameters in obese children. Korean Circ. J. 2010, 40, 179–184. [Google Scholar] [CrossRef] [Green Version]
  25. Blüher, S.; Petroff, D.; Wagner, A.; Warich, K.; Gausche, R.; Klemm, T.; Wagner, M.; Keller, A. The one year exercise and lifestyle intervention program KLAKS: Effects on anthropometric parameters, cardiometabolic risk factors and glycemic control in childhood obesity. Metab. Clin. Exp. 2014, 63, 422–430. [Google Scholar] [CrossRef] [PubMed]
  26. Genoni, G.; Menegon, V.; Monzani, A.; Archero, F.; Tagliaferri, F.; Mancioppi, V.; Peri, C.; Bellone, S.; Prodam, F. Healthy Lifestyle Intervention and Weight Loss Improve Cardiovascular Dysfunction in Children with Obesity. Nutrients 2021, 13, 1301. [Google Scholar] [CrossRef] [PubMed]
  27. Hansen, P.R.; Andersen, L.J.; Rebelo, A.N.; Brito, J.; Hornstrup, T.; Schmidt, J.F.; Jackman, S.R.; Mota, J.; Rêgo, C.; Oliveira, J.; et al. Cardiovascular effects of 3 months of football training in overweight children examined by comprehensive echocardiography: A pilot study. J. Sports Sci. 2013, 31, 1432–1440. [Google Scholar] [CrossRef]
  28. Woo, K.S.; Chook, P.; Yu, C.W.; Sung, R.Y.; Qiao, M.; Leung, S.S.; Lam, C.W.; Metreweli, C.; Celermajer, D.S. Effects of diet and exercise on obesity-related vascular dysfunction in children. Circulation 2004, 109, 1981–1986. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Calcaterra, V.; Palombo, C.; Malacarne, M.; Pagani, M.; Federico, G.; Kozakova, M.; Zuccotti, G.; Lucini, D. Interaction between Autonomic Regulation, Adiposity Indexes and Metabolic Profile in Children and Adolescents with Overweight and Obesity. Children 2021, 8, 686. [Google Scholar] [CrossRef]
  30. World Health Organization. Child Growth Standards. 2006. Available online: https://www.who.int/tools/child-growth-standards (accessed on 1 November 2022).
  31. Maffeis, C.; Banzato, C.; Talamini, G. Obesity Study Group of the Italian Society of Pediatric Endocrinology and Diabetology Waist-to-height ratio, a useful index to identify high metabolic risk in overweight children. J. Pediatr. 2008, 152, 207–213. [Google Scholar] [CrossRef]
  32. Lopez, L.; Colan, S.D.; Frommelt, P.C.; Ensing, G.J.; Kendall, K.; Younoszai, A.K.; Lai, W.W.; Geva, T. Recommendations for quantification methods during the performance of a pediatric echocardiogram: A report from the Pediatric Measurements Writing Group of the American Society of Echocardiography Pediatric and Congenital Heart Disease Council. J. Am. Soc. Echocardiogr. 2010, 23, 465–495; quiz 576–577. [Google Scholar] [CrossRef]
  33. Foster, B.J.; Mackie, A.S.; Mitsnefes, M.; Ali, H.; Mamber, S.; Colan, S.D. A novel method of expressing left ventricular mass relative to body size in children. Circulation 2008, 117, 2769–2775. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Pettersen, M.D.; Du, W.; Skeens, M.E.; Humes, R.A. Regression equations for calculation of z scores of cardiac structures in a large cohort of healthy infants, children, and adolescents: An echocardiographic study. J. Am. Soc. Echocardiogr. 2008, 21, 922–934. [Google Scholar] [CrossRef]
  35. Levy, P.T.; Machefsky, A.; Sanchez, A.A.; Patel, M.D.; Rogal, S.; Fowler, S.; Yaeger, L.; Hardi, A.; Holland, M.R.; Hamvas, A.; et al. Reference Ranges of Left Ventricular Strain Measures by Two-Dimensional Speckle-Tracking Echocardiography in Children: A Systematic Review and Meta-Analysis. J. Am. Soc. Echocardiogr. 2016, 29, 209–225.e6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Ardissino, G.; Ghiglia, S.; Salice, P.; Perrone, M.; Piantanida, S.; De Luca, F.L.; Di Michele, S.; Filippucci, L.; Dardi, E.R.A.; Bollani, T.; et al. Multiple office blood pressure measurement: A novel approach to overcome the weak cornerstone of blood pressure measurement in children. Data from the SPA project. Pediatr. Nephrol. 2020, 35, 687–693. [Google Scholar] [CrossRef] [PubMed]
  37. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: Guidelines for the six-minute walk test. Am. J. Respir. Crit Care Med. 2002, 166, 111–117. [Google Scholar] [CrossRef] [PubMed]
  38. Vandoni, M.; Correale, L.; Puci, M.V.; Galvani, C.; Codella, R.; Togni, F.; La Torre, A.; Casolo, F.; Passi, A.; Orizio, C.; et al. Six minute walk distance and reference values in healthy Italian children: A cross-sectional study. PLoS ONE 2018, 13, e0205792. [Google Scholar] [CrossRef]
  39. Carnevale Pellino, V.; Giuriato, M.; Ceccarelli, G.; Codella, R.; Vandoni, M.; Lovecchio, N.; Nevill, A.M. Explosive Strength Modeling in Children: Trends According to Growth and Prediction Equation. Appl. Sci. 2020, 10, 6430. [Google Scholar] [CrossRef]
  40. Fernandez-Santos, J.R.; Ruiz, J.R.; Cohen, D.D.; Gonzalez-Montesinos, J.L.; Castro-Piñero, J. Reliability and Validity of Tests to Assess Lower-Body Muscular Power in Children. J. Strength Cond Res. 2015, 29, 2277–2285. [Google Scholar] [CrossRef]
  41. Donncha, C.M.; Watson, A.W.S.; McSweeney, T.; O’Donovan, D.J. Reliability of Eurofit Physical Fitness Items for Adolescent Males with and without Mental Retardation. Adapt. Phys. Act. Q. 1999, 16, 86–95. [Google Scholar] [CrossRef]
  42. Tomkinson, G.; Olds, T. Field tests of fitness. In Paediatric Exercise Science and Medicine, 2nd ed.; Armstrong, N., Van Mechelen, W., Eds.; Oxford University Press: Oxford, UK, 2008; pp. 109–128. [Google Scholar]
  43. Ruiz, J.R.; Castro-Piñero, J.; España-Romero, V.; Artero, E.G.; Ortega, F.B.; Cuenca, M.M.; Jimenez-Pavón, D.; Chillón, P.; Girela- Rejón, M.J.; Mora, J.; et al. Field-Based Fitness Assessment in Young People: The ALPHA Health-Related Fitness Test Battery for Children and Adolescents. Br. J. Sports Med. 2011, 45, 518–524. [Google Scholar] [CrossRef]
  44. Vandoni, M.; Carnevale Pellino, V.; Gatti, A.; Lucini, D.; Mannarino, S.; Larizza, C.; Rossi, V.; Tranfaglia, V.; Pirazzi, A.; Biino, V.; et al. Effects of an Online Supervised Exercise Training in Children with Obesity during the COVID-19 Pandemic. Int. J. Environ. Res. Public Health 2022, 19, 9421. [Google Scholar] [CrossRef] [PubMed]
  45. Lamb, K.L. Children’s Ratings of Effort during Cycle Ergometry: An Examination of the Validity of Two Effort Rating Scales. Pediatric Exerc. Sci. 1995, 7, 407–421. [Google Scholar] [CrossRef]
  46. Meng, C.; Yucheng, T.; Shu, L.; Yu, Z. Effects of school-based high-intensity interval training on body composition, cardiorespiratory fitness and cardiometabolic markers in adolescent boys with obesity: A randomized controlled trial. BMC Pediatr. 2022, 22, 112. [Google Scholar] [CrossRef]
  47. Schwingshandl, J.; Sudi, K.; Eibl, B.; Wallner, S.; Borkenstein, M. Effect of an individualised training programme during weight reduction on body composition: A randomised trial. Arch. Dis. Child. 1999, 81, 426–428. [Google Scholar] [CrossRef] [PubMed]
  48. Son, W.M.; Sung, K.D.; Bharath, L.P.; Choi, K.J.; Park, S.Y. Combined exercise training reduces blood pressure, arterial stiffness, and insulin resistance in obese prehypertensive adolescent girls. Clin. Exp. Hypertens. 2017, 39, 546–552. [Google Scholar] [CrossRef] [PubMed]
  49. Shih, K.C.; Kwok, C.F. Exercise reduces body fat and improves insulin sensitivity and pancreatic β-cell function in overweight and obese male Taiwanese adolescents. BMC Pediatr. 2018, 18, 80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Hardy, C.J.; Rejeski, W.J. Not What, but How One Feels: The Measurement of Affect during Exercise. J. Sport Exerc. Psychol. 1989, 11, 304–317. [Google Scholar] [CrossRef]
  51. Ferrante, A.W., Jr. Obesity-induced inflammation: A metabolic dialogue in the language of inflammation. J. Intern. Med. 2007, 262, 408–414. [Google Scholar] [CrossRef]
  52. Tian, D.; Meng, J. Exercise for Prevention and Relief of Cardiovascular Disease: Prognoses, Mechanisms, and Approaches. Oxidative Med. Cell. Longev. 2019, 2019, 3756750. [Google Scholar] [CrossRef] [Green Version]
  53. Niemiro, G.M.; Rewane, A.; Algotar, A.M. Exercise and Fitness Effect On Obesity. In StatPearls; StatPearls Publishing: Tampa, FL, USA, 2022. Available online: https://www.ncbi.nlm.nih.gov/books/NBK539893. (accessed on 5 January 2023).
  54. Krawczewski Carhuatanta, K.A.; Demuro, G.; Tschöp, M.H.; Pfluger, P.T.; Benoit, S.C.; Obici, S. Voluntary exercise improves high-fat diet-induced leptin resistance independent of adiposity. Endocrinology 2011, 152, 2655–2664. [Google Scholar] [CrossRef]
  55. Valerio, G.; Maffeis, C.; Saggese, G.; Ambruzzi, M.A.; Balsamo, A.; Bellone, S.; Bergamini, M.; Bernasconi, S.; Bona, G.; Calcaterra, V.; et al. Diagnosis, treatment and prevention of pediatric obesity: Consensus position statement of the Italian Society for Pediatric Endocrinology and Diabetology and the Italian Society of Pediatrics. Ital. J. Pediatr. 2018, 44, 88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Yang, H.; Wright, L.; Negishi, T.; Negishi, K.; Liu, J.; Marwick, T.H. Research to Practice: Assessment of Left Ventricular Global Longitudinal Strain for Surveillance of Cancer Chemotherapeutic-Related Cardiac Dysfunction. JACC Cardiovasc Imaging 2018, 11, 1196–1201. [Google Scholar] [CrossRef]
  57. Soare, R.; Brasil, I.; Monteiro, W.; Farinatti, P. Effects of physical activity on body mass and composition of school-age children and adolescents with overweight or obesity: Systematic review focusing on intervention characteristics. J. Bodyw. Mov. Ther. 2023, 33, 154–163. [Google Scholar] [CrossRef]
  58. Cvetković, N.; Stojanović, E.; Stojiljković, N.; Nikolić, D.; Scanlan, A.T.; Milanović, Z. Exercise training in overweight and obese children: Recreational football and high-intensity interval training provide similar benefits to physical fitness. Scand J. Med. Sci. Sports 2018, 28, 18–32. [Google Scholar] [CrossRef] [PubMed]
  59. Valeriani, F.; Protano, C.; Marotta, D.; Liguori, G.; Romano Spica, V.; Valerio, G.; Vitali, M.; Gallè, F. Exergames in Childhood Obesity Treatment: A Systematic Review. Int. J. Environ. Res. Public Health 2021, 18, 4938. [Google Scholar] [CrossRef]
  60. Powell, B.D.; Redfield, M.M.; Bybee, K.A.; Freeman, W.K.; Rihal, C.S. Association of obesity with left ventricular remodeling and diastolic dysfunction in patients without coronary artery disease. Am. J. Cardiol. 2006, 98, 116–120. [Google Scholar] [CrossRef] [PubMed]
  61. Abel, E.D.; Litwin, S.E.; Sweeney, G. Cardiac remodeling in obesity. Physiol. Rev. 2008, 88, 389–419. [Google Scholar] [CrossRef] [PubMed]
  62. Obert, P.; Mandigout, S.; Vinet, A.; N’Guyen, L.D.; Stecken, F.; Courteix, D. Effect of aerobic training and detraining on left ventricular dimensions and diastolic function in prepubertal boys and girls. Int. J. Sports Med. 2001, 22, 90–96. [Google Scholar] [CrossRef]
  63. Hayashi, T.; Fujino, M.; Shindo, M.; Hiroki, T.; Arakawa, K. Echocardiographic and electrocardiographic measures in obese children after an exercise program. Int. J. Obes. 1987, 11, 465–472. [Google Scholar]
  64. Krustrup, P.; Hansen, P.R.; Nielsen, C.M.; Larsen, M.N.; Randers, M.B.; Manniche, V.; Hansen, L.; Dvorak, J.; Bangsbo, J. Structural and functional cardiac adaptations to a 10-week school-based football intervention for 9–10-year-old children. Scand. J. Med. Sci. Sport. 2014, 24, 4–9. [Google Scholar] [CrossRef]
Table 1. Baseline data of the enrolled pediatric patients. Quantitative variables are expressed as the mean (±standard deviation, SD) and categorical variables are described as counts and percentages.
Table 1. Baseline data of the enrolled pediatric patients. Quantitative variables are expressed as the mean (±standard deviation, SD) and categorical variables are described as counts and percentages.
Baseline CharacteristicsTime T0Time T1
Patient numbers (n)2727
Age (years)11.0 ± 2.011.2 ± 2.0
Gender -
 Male, n (%)18 (67)
 Female, n (%)9 (33)
Pubertal stages
 Prepubertal, n (%)16 (59.3)14 (51.8)
 Middle puberty, n (%)5 (18.5)7 (25.9)
 Late puberty, n (%)6 (22.2)6 (22.2)
Ethnicity -
 White, non-Hispanic, n (%)17 (63)
 Afroamerican, n (%)4 (15)
 Hispanic or Latino, n (%)6 (22)
Weight, kg65.57 ± 11.0366.56 ± 10.89
Weight, z-score1.97 ± 0.221.97 ± 0.52
Height, cm149.9 ± 6.58152.1 ± 4.95
Height, z-score0.48 ± 1.20.59 ± 1.4
Body mass index, kg/m226.3 ± 0.626.0 ± 1.4
Body mass index, z-score2.16 ± 0.52.03 ± 0.6
Waist circumference, cm90.5 ± 11.288.6 ± 10.8
Waist circumference/height ratio0.61 ± 0.050.58 ± 0.04
Table 2. Comparison between blood pressure measurements at baseline (T0) and after training (T1). Data are expressed as the mean (±standard deviation, SD). Z-scores are expressed as the mean (±SD).
Table 2. Comparison between blood pressure measurements at baseline (T0) and after training (T1). Data are expressed as the mean (±standard deviation, SD). Z-scores are expressed as the mean (±SD).
ParametersT0T1p-Value
Systolic pressure (mmHg)
 Mean (±SD)117.0 ± 9.7113.6 ± 10.30.05
 Z-score, mean (±SD)1.15 ± 0.840.82 ± 0.930.027
 Centiles (±SD)80.89 ± 17.8272.44 ± 23.440.063
Diastolic pressure (mmHg)
 Mean (±SD)69.3 ± 8.164.0 ± 7.00.001
 Z-score, mean (±SD)0.68 ± 0.670.16 ± 0.57<0.001
 Centiles (±SD)70.07 ± 21.0955.56 ± 20.310.001
Mean arterial pressure (mmHg)
Mean (±SD)85.2 ± 7.980.5 ± 7.40.002
Table 3. Comparison between the echocardiographic data at baseline (T0) and after training (T1). Data are expressed as the mean (±standard deviation, SD). Z-scores are expressed as the mean (±SD).
Table 3. Comparison between the echocardiographic data at baseline (T0) and after training (T1). Data are expressed as the mean (±standard deviation, SD). Z-scores are expressed as the mean (±SD).
Echocardiographic VariablesT0
(n = 27)
T1
(n = 27)
p-Value
RV systolic function
 RVFWLS (%)−23.9 (±2.1)−23.7 (±2.4)0.610
LV systolic function
 LV GLS (%)−22.5 (±1.5)−23.5 (±1.9)0.016
LV diastolic function
 E/e’5.79 (±0.78)5.82 (±0.74)0.856
 LAS (%)41.1 (±5.4)41.1 (±4.93)0.975
LV measurements
 EDD (mm)42.5 (±3.7)43.3 (±4.0)0.045
 EDD z-score−1.09 (±1.05)−1.01 (±1.06)0.435
 IVSd (mm)7.84 (±0.96)7.63 (±0.94)0.011
 IVSd z-score0.19 (±0.48)−0.001 (±0.41)0.001
 PWd (mm)7.55 (±0.84)7.47 (±0.82)0.239
 PWd z-score 0.41 (±0.59)0.27 (±0.58)0.017
 LV mass indexed for height (g/m2.7)33.61 (±6.35)32.23 (±5.36)0.393
RV (right ventricle), RVFWLS (right ventricle free wall longitudinal strain), LV (left ventricle), LV GLS (left ventricle global longitudinal strain), LAS (left atrium strain), EDD (end-diastolic diameter), IVSd (interventricular septum diastolic), and PWd (posterior wall diastolic).
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Mannarino, S.; Santacesaria, S.; Raso, I.; Garbin, M.; Pipolo, A.; Ghiglia, S.; Tarallo, G.; De Silvestri, A.; Vandoni, M.; Lucini, D.; et al. Benefits in Cardiac Function from a Remote Exercise Program in Children with Obesity. Int. J. Environ. Res. Public Health 2023, 20, 1544. https://doi.org/10.3390/ijerph20021544

AMA Style

Mannarino S, Santacesaria S, Raso I, Garbin M, Pipolo A, Ghiglia S, Tarallo G, De Silvestri A, Vandoni M, Lucini D, et al. Benefits in Cardiac Function from a Remote Exercise Program in Children with Obesity. International Journal of Environmental Research and Public Health. 2023; 20(2):1544. https://doi.org/10.3390/ijerph20021544

Chicago/Turabian Style

Mannarino, Savina, Sara Santacesaria, Irene Raso, Massimo Garbin, Andreana Pipolo, Silvia Ghiglia, Gabriele Tarallo, Annalisa De Silvestri, Matteo Vandoni, Daniela Lucini, and et al. 2023. "Benefits in Cardiac Function from a Remote Exercise Program in Children with Obesity" International Journal of Environmental Research and Public Health 20, no. 2: 1544. https://doi.org/10.3390/ijerph20021544

APA Style

Mannarino, S., Santacesaria, S., Raso, I., Garbin, M., Pipolo, A., Ghiglia, S., Tarallo, G., De Silvestri, A., Vandoni, M., Lucini, D., Carnevale Pellino, V., Bernardelli, G., Gatti, A., Rossi, V., Calcaterra, V., & Zuccotti, G. (2023). Benefits in Cardiac Function from a Remote Exercise Program in Children with Obesity. International Journal of Environmental Research and Public Health, 20(2), 1544. https://doi.org/10.3390/ijerph20021544

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