Altered cardiovascular autonomic regulation in overweight children engaged in regular physical activity
- Daniela Lucini1,2,
- Gaia de Giacomi2,
- Fabio Tosi1,3,
- Mara Malacarne1,
- Stefano Respizzi2,
- Massimo Pagani1,3
- 1Centro di ricerca Terapia Neurovegetativa e Medicina dell'esercizio, Dipartimento Scienze Cliniche, Università degli Studi di Milano, Milano, Italy
- 2Dipartimento di RiabiIazione e Recupero Funzionale, IRCCS Istituto Clinico Humanitas, Rozzano, Italy
- 3U.O. Telemedicina e Medicina dello Sport, Ospedale “Luigi Sacco”, Milano, Italy
- Correspondence to Dr Daniela Lucini, Dipartimento di Riabilitazione e Recupero Funzionale, IRCCS Istituto Clinico Humanitas, Rozzano, Italy;
- Received 28 June 2012
- Revised 11 September 2012
- Accepted 18 September 2012
- Published Online First 19 October 2012
Overweight (OW) and obesity in children are important forerunners of cardiovascular risk, possibly through autonomic nervous system (ANS) dysregulation, while physical exercise exerts a beneficial influence. In this observational study we hypothesise that OW might influence ANS profile even in a population performing high volume of supervised exercise. We study 103 young soccer players, homogeneous in terms of gender (all male), cultural background, school, age (11.2±1 years) and exercise routine, since they all belong to the same soccer club, thus guaranteeing equality of supervised training and similar levels of competitiveness. ANS is evaluated by autoregressive spectral analysis of heart rate and systolic arterial pressure (SAP) variabilities. We estimate also the accumulated weekly Metabolic Equivalents and time spent in sedentary activities. We subdivide the entire population in two subgroups (normal weight and OW) based on the International Obesity Task Force criteria. In OW soccer players (10.7% of total group) we observe an altered profile of autonomic cardiovascular regulation, characterised by higher values of SAP (113±4 vs 100±1 mm Hg, 39.7±3 vs 66.2±10%), higher Low Frequency variability power of SAP (an index of vasomotor sympathetic regulation) (12±3 vs 4.5 mm Hg2) and smaller spontaneous baroreflex gain (an index of cardiac vagal regulation) (19±3 vs 33 ±3 ms/mm Hg) (all (p<0.02)). Moreover Correlation analysis on the entire study population shows a significant link between anthropometric and autonomic indices. These data show that OW is associated to a clear autonomic impairment even in children subjected to an intense aerobic training.
According to international guidelines, in order to promote health, children should engage in at least 60 min of moderate–vigorous physical activity most if not all days of the week.1–3 Regular physical activity implies an immediate and long-term improvement in health measures, such as easier maintenance of correct weight and metabolic profile, improved cardiovascular health and enhanced well-being, reducing the risk of eventually developing obesity and diabetes later in life.1–3 Activity should also be fun, and enjoyable to facilitate acceptance and maintenance of the routine.1 ,4 In fact, it is well recognised that a large fraction of children, typically when reaching adolescence, abandon sport activities5 ,6 for various reasons: for example, because school programmes become more onerous and strive for time dedicated to other more leisurely activities, or rewards of competitions remain below the level they had hoped for and children become disillusioned, or because other leisure time activities become more desirable. Accordingly programmes directed to children with the aim to initiate and maintain an active life through adulthood2 ,4 ,7 should not only focus on obtaining momentary participation to sport but also favour the emergence of an active mentality.4 ,8–10 In the context of modern, largely sedentary society, supervised sport activities might be preferable to simple spontaneous activity, as they are easier to monitor and to introduce into standard school programmes, thus favouring the development of an active culture.11 Such paradigm shift might be critical to counter the growing tendency to sedentariness that is observed in children, and which might favour the present epidemic of obesity.9 ,12 Overweight (OW) and obesity are important forerunners of essentially all altered functional elements of the cardiovascular risk profile: from arterial pressure,13 or metabolic control12 as well as autonomic cardiovascular regulation,14 ,15 while physical exercise exerts a beneficial influence.16 ,17
Supporting evidence is irrefutable in adults,18 but only recent investigations in children14 ,15 suggest that frank obesity might induce an autonomic dysregulation also in a paediatric population, while data regarding simple OW are less cogent. It is also unknown whether practicing high volume of physical exercise exerts a protective effect on autonomic and metabolic regulation in children.
In Italy, soccer represents the most appealing sport for children, particularly boys, who consider it highly enjoyable. Young players are organised by sport Clubs, which are responsible for running facilities and for the organisation of training and competitions within the framework of the Italian National Olympic Committee. Clubs also are responsible of fostering players' health by organising the yearly mandatory Preparticipation Screening19 ,20 and possibly other health programmes. Conversely there is a substantial lack of structured physical activity programmes in Italian school curricula.
In this context we planned the present observational study on a unique group of young male soccer players all belonging to the same football club (ADS Rozzano Calcio), and thus rigorously subjected to the same intense exercise training.
The present proof of concept investigation is based on the likely hypothesis that in the study group a small fraction of children could be found OW, because of the observation that in northern Italy prevalence of obesity and OW in the general paediatric population is of the order of 20%.21
The specific aim is to assess whether cardiac baroreflex and vascular autonomic indices are altered in the OW subpopulation of active young football players. A positive result would support the feasibility of introducing non-invasive autonomic cardiovascular regulation assessment as a means to monitor the beneficial effects of exercise and other lifestyle interventions in school age children.
This observational study involves 103 boys (age 11.1±1.0 years) that accessed the outpatient clinic of the Department of Rehabilitation of Istituto Clinico Humanitas in Milan, Italy, as part of a health screening programme planned for ADS Rozzano Calcio Club, intended to test the health status of all boys enrolled in the junior team as an additional benefit to young football players. All boys are subjected to the same training routine, consisting of three structured sessions per week of 1.5 h (endurance training at moderate/vigorous intensity) and one soccer game/week of at least 1 h. The protocol followed the principles of the Declaration of Helsinki and Title 45, US Code of Federal Regulations, Part 46, Protection of Human Subjects, Revised 13 November 2001, effective 13 December 2001 and was approved by the Institutional Ethics Committee. All participants’ parents gave their informed consent.
General average characteristics are presented in table 1. In all subjects the presence of clinical evidence of disease or pharmacological treatment was excluded by history and standard medical examination. Note also that all subjects had previously been certified fit at the yearly mandatory Preparticipation Screening.19 ,20 The International Obesity Task Force criteria22 were used to define OW and obesity. These criteria identify gender-adjusted and age-adjusted body mass index (BMI) values associated with a predicted BMI of 25 kg/m2 (OW) and 30 kg/m2 (obesity) at the age of 18 years. Moreover, individual weight, height and BMI percentiles are assessed using charts available online from the Center for Disease Control and Prevention (CDC) (http://www.cdc.gov/growthcharts): OW is considered in the range the 85–94% BMI and obesity beyond 95% BMI.1 Blood pressure percentiles were calculated using the chart available online (http://www.bcm.edu/bodycomplab/Flashapps/BPVAgeChartpage.html) from the Baylor College of medicine.
Autonomic and baroreflex assessment
The day of the study all subjects arrived in the clinic at least 2 h after a light meal, avoiding caffeinated beverages and heavy physical exercise in the preceding 24 h. Recordings were performed between 16:00 and 19:00, to account for school duties and avoid influences of circadian variations on autonomic function.
After a preliminary 10-min rest period in supine position, allowed for stabilisation, blood pressure waveforms, ECG and respiratory activity were continuously recorded over a 10-min baseline. The ECG (CM5) and the respiratory signal were recorded in all subjects with a two-way radiotelemetry system (Marazza, Monza Italy), while arterial pressure waveform was continuously assessed non-invasively by Finapres device (Finapres, Ohmeda, Englewood, Colorado, USA), the accuracy of which in tracking beat by beat blood pressure changes has been previously documented.23 Data were acquired with a PC at 250 samples/channel/second.
As described previously,24 ,25 from the simultaneous autoregressive spectral analysis of RR interval and systolic arterial pressure (SAP) variability, a series of indexes indirectly reflecting autonomic cardiovascular modulation were derived. RR interval spectral powers were quantified in the low frequency (LF, 0.03–0.14 Hz) and in the high frequency (HF, 0.15–0.35 Hz) regions. LF spectral powers were normalised according to the formula PLF(nu)=((PLF(msec)2)/(VARRR(msec)2−VLF(msec)2))*100 (where PLF(nu)=LF powers in normalised unit, VAR=total variance; VLF=very low frequency component, <0.03 Hz); similar normalisation was performed for HF powers. LF/HF of RR interval variability power ratio was also computed. The resting balance between LF and HF oscillatory components of RR variability (particularly using normalised units (nu)) reflects the changing dynamics of, respectively, sympathetic and vagal oscillatory modulation of the Sino Atrial (SA) node.
SAP spectral powers were quantified in the LF region (LF, 0.03–0.14 Hz) and reported in absolute units,26 as an index of sympathetic arterial blood pressure modulation. The sensitivity of spontaneous arterial baroreflex control of RR interval was assessed by a frequency domain method (α index=average of square root of the ratio between RR interval and SAP Spectral powers in the LF and HF regions),25 and with a time domain method (Baroreflex slope).27 Baroreflex gain provides an index of vagal cardiac regulation, particularly useful in assessing exercise training effects.28
All boys and parents were interviewed by a trained physician who used a semistructured questionnaire.29 We use more recent guidelines recommendation2 ,30 ,31 in order to estimate the dose of physical activity performed. We assess17 the time spent every week walking (at least 10 min consecutively) or doing moderate or vigorous exercise both for structured exercise or leisure-time physical activities, and we use conversion factors4 ,30 ,31 to estimate the amount of accumulated Metabolic Equivalents (METs). We also assess sedentary behaviour, beyond sleep and regular school activity, quantifying the time spent doing school homework, watching TV, using personal computers or electronic games and on private or public transportations.9 The questionnaire also contained an item relative to reasons for playing football, and other lifestyle items not relevant to the present investigation. The validity of this approach, based on self-reports, has been recently documented.29
Data are presented as mean±SEM.
Significance of differences between the normal weight (NW) and OW groups was assessed with a non-paired T test. Significance level was set at p<0.05, two sided. Bivariate Spearman correlations were also calculated for most relevant variables. Automatic linear regression, providing significance and importance of variables, was also employed to assess multivariate relationships. All computations were performed with a commercial statistical package (SPSS V.19).
Eleven subjects (10.7%) of the entire group were OW. Table 1 reports summary data describing anthropometrics and physical activity habits of the study population, subdivided in two considered groups: NW and OW. Since the training and competition routine set by Rozzano Calcio club was exactly the same for all children, there are no differences between groups regarding weekly reported active time and attendant estimated METS, while a slight, not significantly greater sedentary time was reported for OW. Significantly greater values of body weight (both in kg and percentiles), of Body Mass Index (both in kg/m2 and percentiles) and of abdominal circumference, are observed in the small group of OW players as compared to NW.
Table 2 and figure 1 demonstrate the autonomic profile as provided by RR and SAP variability indices. Similar values are observed in the two groups regarding measures of RR variability (both in absolute and normalised units), while SAP (but not diastolic pressure) (expressed both in mm Hg and in percentiles), its variance and absolute power of its LF component (LFSAP) are significantly greater in OW. No difference is observed for the HF SAP power (not reported for simplicity). Simultaneously, values of spontaneous baroreflex, either from frequency (index α) and time domains (Baroreflex slope) measures are smaller in the OW group.
Correlation analysis on the entire study population (table 3) shows a significant link between anthropometric indices and measures of spontaneous baroreflex and arterial pressure: in particular α index, SAP and its LF component of variability correlate significantly with body weight, body weight %, BMI, BMI % and waist circumference. Automatic linear modelling shows in the case of index α a clear significance for body weight (p=0.007, importance 0.511) and borderline for total METS; in the case of LFSAP there is a strong significant effect with BMI% (p<0.002; importance 0.523) and borderline with SAP%.
The novel finding of this study is that in a small group of young competitive OW soccer players, in spite of being exposed to a relatively heavy training routine, we observe an altered profile of autonomic cardiovascular regulation, characterised by higher values of SAP, higher LF variability power of SAP (an index of vasomotor sympathetic regulation) and reduced spontaneous baroreflex gain (an index of cardiac vagal regulation).
Exercise load, body weight and early cardiovascular risk in children
In Italy about 60% of children of 11–14 years of age participate regularly to some form of activity, and slightly less than a third (about 14%) participate to intense, organised sport.21 ,32 Of these a majority (about a total of 41%) declares to practice soccer, which results the preferred sport, particularly among boys. The large number of young soccer players facilitates the appearance of organised clubs, under the auspices of the Italian Olympic Committee. Clubs organise training, and the participation to regular competitions. These activities favour the emergence of a sport mentality, and might limit the abandonment of sport practice typically reported to occur at the turn of adolescence.5 Conversely the maintenance of an active lifestyle might play a key role in avoiding the increase in BMI with aging.7 ,33 ,34 An active lifestyle might also play a role in avoiding or limiting age-related increases in arterial pressure and optimising the metabolic profile.35 Recent epidemiological evidence shows in the context of the obesity epidemic the emergence of risky cardiovascular profiles also in children who beyond OW might carry the full blown metabolic syndrome or diabetic phenotype.1 ,10 ,12 Given these premises, the observation that a sizable fraction (about 10%) of young soccer players, in spite of a heavy activity load, falls into the OW percentiles and demonstrates greater abdominal circumference36 (a surrogate measure of abdominal fat) than their normoweight club mates, calls for special attention in view of the critical role that abdominal obesity might play in the setting of cardiovascular risk. In this study we do not explore the potential reasons for this specific abnormality; accordingly, investigation on eating habits was limited to simple enquiry of few recognised aspects of diet,2 which were found similar in the two considered populations. Importantly though, in relation to elements of cardiovascular risk, OW children show SAP values higher than found in their normoweight counterpart. In view of the well-known hypotensive effects of aerobic training in adults3 ,17 we might also argue that the excessive arterial pressure load related to OW (table 3) could have been more apparent had these children not practiced the reported intense physical training. An additional role of sedentariness cannot be fully demonstrated because the sedentary time results only marginally greater in the OW group, yet the significant correlation of sedentary time with body weight and with waist circumference (respectively r=0.486 p≪0.001 and r≪0.369 p=0.001) in the entire group would speak in favour of planning further research about this link. A critical role of inactivity as a component of risk is indeed reported not only in adults9 ,37 ,38 but also recently in children.39 ,40 Because of the study design considering children all subjected to the same heavy routine, differences between groups in measures of activity are absent.
Cardiovascular autonomic regulation, overweight and soccer in children
Although altered autonomic regulation is a well known companion of obesity and OW, the mechanisms by which excess weight favours autonomic dysfunction, in spite of ongoing work of many laboratories, are still incompletely understood. Alterations of several intertwined functional elements might be involved, such as inflammation41 and impaired endothelial function,42 insulin resistance,43 impaired glucose tolerance,44 dysfunctional leptin45 and ghrelin regulation,46 leading to an increase in sympathetic activity,18 ,47 a reduction of cardiac baroreflex sensitivity,48 and also facilitating an increase in arterial pressure. These autonomic changes are also forerunners of increased cardiovascular risk profile in a wide range of conditions, including hypertension,49 congestive heart failure and coronary artery disease.50 Studies on children thus provide a unique window on the beginnings of a lifelong history of changes in cardiovascular autonomic regulation. For example, a reduction of baroreflex gain is observed in children with prehypertension51 and, complemented by an augmented LF power of SAP variability, also in children affected by early type 1 diabetes52 and in obese sedentary children.14 ,15
Accordingly the observation of a complex initial autonomic dysregulation in the subgroup of young OW soccer players might bear relevance not so much to present day practice but rather particularly regarding cardiovascular prevention in the future.7 ,12 ,52 ,53 Indeed on one hand these data suggest that soccer training per se is not sufficient to fully protect from OW and attendant autonomic alterations; secondly, there might be a link between idle time spent sedentary, and anthropometric indices of OW. In consideration of the characteristics of the protocol, we do not delve into the mechanisms of the positive relationship between sedentariness and weight, although it might be argued that both genetic54 (eg, OW parents) and environmental factors (TV viewing or computer time) could be implicated.37 ,40
In order to focus the possible clinical implications of autonomic differences between NW and OW groups, we should also consider that in the latter group we also observe greater values in arterial pressure. Indeed, in a prior study in hypertensive children51 we observed a reduction of baroreflex gain, and a change in indices of RR variability, suggesting a prevailing sympathetic oscillatory modulation of the SA node.49 ,55 It might be tempting to speculate that the greater sedentariness observed in hypertensive children51 might play a role in favouring the observed predominance of indices of sympathetic oscillatory modulation. A reduced baroreflex gain, increase in arterial pressure and in arterial pressure variability was associated to increased left ventricular mass in children with obstructive sleep apnoea.56 The observation that an increase in the LF component of SAP variability was associated to reduced baroreflex gain also in children with type 1 diabetes,52 as well as in children with frank obesity,14 ,15 suggests that overall the combination of reduced cardiac vagal regulation of the SA node and disturbed sympathetic vascular regulation might be a more general hallmark of initial autonomic derangements in children with metabolic imbalance, such as OW. In this context it may be important to note that such alterations are present in this group of children in spite of an intense training in competitive sport, suggesting that its origin is likely to be complex and multifactorial.
This is an observational study on a relatively small group of children, who are however highly homogeneous in terms of gender (all male), cultural background, age and exercise routine, since they all belong to the same soccer club, thus guaranteeing equality of supervised training and similar levels of competitiveness. Such unique set of data seems to fall into the category of findings that, although limited in statistical power because of small number of cases (N), are likely to provide valuable information on a new area of investigation justifying their dissemination.57
Because of design and ethical considerations, clinical data are limited to standard history, and physical examination, although the good health of each participant is corroborated by the repeated preparticipation health assessments, as requested by Italian law.
A fraction of lifestyle data (particularly exercise and sedentary time) is obtained through questionnaires and self reports whose accuracy may be questioned by some investigators. A similar questionnaire has been used and tested in a recent survey on a population of workers, and found reliable, particularly when the participants (or, as in this case, their parents) found a vested interest in obtaining correct data.29 However reliance on self reports of physical activity, particularly in the case of children, might be rather imperfect, and even partly obscure important aspects, such as the key role of inactivity during everyday life. Such a limitation could be overcome by the use of more modern motion sensors.
Finally we must emphasise that a single point observation lacks the strength of a longitudinal study. However these preliminary observations might furnish a rational basis to design more robust investigations on the beneficial effects of sport, such as soccer, as a lifestyle treatment for early cardiovascular autonomic dysregulation.
What are the new findings
Young competitive soccer players, in spite of being exposed to a relatively heavy training routine, might be overweight (OW).
In OW young soccer players we observe an altered profile of autonomic cardiovascular regulation, and slightly higher values of systolic arterial pressure.
Observation of an initial autonomic dysregulation in young OW soccer players might bear relevance not so much to present day practice but rather to cardiovascular prevention in the future.
Our data suggest that soccer training per se is not sufficient to fully protect from OW and attendant autonomic alterations
How might it impact on clinical practice in the near future
Our data support the position that
Sport should be combined with education on other life health issues, particularly regarding nutrition on the basis that soccer training per se is not sufficient to fully protect from overweight.
Overweight even combined with heavy exercise loads might initiate since childhood negative cardiovascular and autonomic changes leading to increased risk later on in life.
These alterations can be detected with simple non-invasive measurements that could be considered for inclusion in the yearly health screening as a guide to individual prevention.
The untiring secretarial help of Giovanna Maccio’ is gratefully acknowledged.
Contributors DL, SR and MP planned the study; GG and FT collected and analysed data; MM did the autonomic analysis and drafted data summaries; DL and MP drafted the paper; all authors provided comments and final supervision of the text.
Competing interests None.
Source of support ASI contract DCMC.
Patient consent Obtained.
Ethics approval IRCCS IC Humanitas.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement We are willing to share data with interested investigators. Other clinical data is also available to interested scientists.