Background

Obesity in childhood is a strong predictor of adult obesity with health and economic consequences for both the individual and the society [1].

Obesity-related oxidative stress (OS) has been linked to metabolic and cardiovascular disease [2, 3], although this association remains elusive especially in childhood [4, 5].

Recently, we analyzed the relation between circulating oxidized LDL cholesterol (oxLDL) and metabolic syndrome (MetS) in a pediatric population, to define whether plasma oxLDL levels were correlated to obesity and whether oxidative damage, evaluated by assessing oxLDL levels, was associated with MetS [6]. We demonstrated that overweight and obese children showed significantly higher oxLDL levels when compared to normal weight children [6]. Additionally, we found a correlation between oxLDL levels and increased waist/height ratio (WHeR, visceral adiposity marker) in obese children suggesting that oxidative damage was correlated with a hypertriglyceridemic waist phenotype and could be a precocious marker of MetS and thus cardiometabolic risk in obese children [6].

Based on our preliminary findings [6] and considering oxLDL as a sensor of OS in childhood obesity, according to the European Food Safety Authority Panel on Dietetic Products, Nutrition and Allergies [7], in this ancillary short communication, we integrated and related our oxLDL existing results to lifestyle variables of our pediatric population to investigate OS-related lifestyle variable with the purpose to prevent oxidative damage in children affected by overweight/obesity.

Methods

Subjects

This ancillary study, referred to a pediatric population, previously described by Calcaterra et al. [6]. Briefly, 178 Caucasian children and adolescents aged 11.8 ± 2.6 years (88 females and 90 males) were evaluated and classified as normal weight, affected by overweight and obesity, according to age–sex percentiles curves of body mass index (BMI) proposed by Cole [8] (BMI < 75th percentile; BMI 75–97th percentile; BMI > 97th percentile, respectively).

Lifestyle variables assessment

Lifestyle variables collection are recorded at the time of oxLDL analysis [6]. We assessed dietary habits and physical activity using two sections of a previously published questionnaire [9]. Each section consisted of questions (14 questions for dietary habits and 5 questions for physical activity) with the following response categories: always, often, sometimes, never. The score assigned to each response ranged from 0 to 3, with the maximum score assigned to the healthiest one and the minimum score to the least healthy questionnaire [9].

The dietary habits section was designed to investigate the food habits such as breakfast consumption, daily water assumption, daily number of meals, and consumption of fruit, vegetables, and soft drinks or alcoholic beverages [9].

Concerning physical activity, answers were structured to quantify the time spent weekly in physical activity, to investigate the activities spent during the free time (such as walking, watching TV, listening to music, using the computer, reading a book, practicing a sport and shopping), and to quantify the hours spent daily on the computer or in watching TV [9].

This study was conducted according to the Good Clinical Practice guidelines and was approved by the Human Ethics Committee of Fondazione IRCCS Policlinico S. Matteo of Pavia (Protocol number: 20150005231). The informed written consent of a parent or legal guardian was required for subjects aged < 18, and the subjects aged ≥ 8 were asked to give their written assent. Patients’ parents and patients > 8 years gave their written consent to data publication. Ethics Committee also approved data publication.

Statistical analysis

Data quality control and statistical analyses were performed using STATA 11 (StataCorp, College Station, TX, USA). Descriptive statistics representing means and standard error concerning oxLDL levels were computed. A multiple regression analysis was applied to evaluate the association between serum oxLDL levels and total dietary habits and physical activity scores, taking into account the effect of age, sex, BMI and WHeR as possible confounders.

The analysis of variance (ANOVA) was used to verify patients’ characteristics regarding dietary habits and physical activity level.

Results

As previously reported [6], based on the BMI percentiles threshold, 49 of the 178 patients (27.5%) were normal weight, 76 (42.7%) were affected by overweight and 53 (29.8%) were affected by obesity and children with obesity showed higher serum oxLDL levels compared to normal weight and children affected by overweight (p < 0.05).

Considering the total score of dietary habits section, ANOVA analysis reported no significant differences between normal weight children and those affected by either overweight or obesity (Fig. 1a; Table 1).

Fig. 1
figure 1

Box and whisker plots of dietary habits (a) and physical activity (b) scores in the study population. Data are reported as means (error bars: 95% confidence interval for mean)

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Table 1 Total dietary habits and physical activity score among study population
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Fig. 2
figure 2

Estimates of oxLDL levels related to certain items of dietary habits section. Data are presented as mean and standard error (SE)

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Table 2 Influence of certain dietary habits on oxLDL levels
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The worst eating habits were skipping breakfast (about 20% of the sample); 30% did not drink milk or yogurt at breakfast; most subjects did not eat at least two portions of fruit and vegetables every day (80%). In 25% of the sample, consumption of cakes and sweets was too high, always eating a dessert at the end of the meal. Data showed inadequate water consumption (< 1 L/day) in one-third of the sample, with no differences according to BMI nor gender.

Normal weight children reported a significantly higher total physical activity score (p = 0.001) when compared to those of children affected by overweight and obesity (Fig. 1b; Table 1). Since multiple regression analysis reported no correlation between serum oxLDL levels and the total dietary habits and physical activity scores (p = 0.73, r = − 0.022 and p = 0.62, r = − 0.07, respectively), we analyzed the influence of each item of both sections on oxidative damage. BMI-adjusted ANOVA analysis reported significantly increased serum oxLDL levels only in subjects drinking < 1 L/day of water (64.0 ± 5.1 U/L; p = 0.022) in daily consumers of chocolate drinks at breakfast (88.5 ± 16.1; p value = 0.029) and significantly decreased oxLDL levels in subjects consuming a breakfast based mainly on fruits (48.5 ± 16.7; p = 0.004) (Tables 1, 2; Figs. 1a–c, 2). Moreover, as shown in Fig. 1d, e, “high-fat diet” and “always eating a dessert at the end of the meal” were correlated with increased serum oxLDL levels with a trend toward significance (Table 1). As regards physical activity, no correlations were reported.

Discussion

The prevalence of obesity in European and adolescents has increased at an alarming rate, becoming a major public health concern. The determinants for overweight and obesity include unhealthy lifestyle, environmental, familial and societal factors, widely accepted as primary driving forces behind the disease process of, among others, MetS [10].

In this ancillary short communication, we integrated and related our oxLDL existing results previously assessed in children affected by overweight/obesity [6] to lifestyle variables to investigate OS-related lifestyle variables.

Normal weight children and those affected by either overweight or obesity did not differ significantly in dietary habits as previously reported in literature [11]. Thus, eating habits do not show significance differences, despite BMI. On the contrary, normal weight children reported a significantly higher total physical activity score, when compared to those of children affected by overweight and obesity. These findings suggest that physical activity has an important impact on BMI; to be specific, more physical activity is associated with lower BMI scores. Both low sedentary and high exercise activities contribute to increased energy expenditure, improved weight control and prevention of obesity. Exercise, if intensity is at least moderate, has also a positive effect on fat distribution by decreasing the proportion of abdominal and visceral fat [12, 13].

We analyzed the influence of each item of the dietary habits and physical activity scores on oxidative damage, since no correlation was found between serum oxLDL levels and the total scores of both sections.

Results showed significantly increased serum oxLDL levels in subjects drinking < 1 L/day of water. The benefit of water intake lies in the fact that water consumption could replace other caloric beverages and thereby reduce total calories consumed as highlighted in literature [14]. In a recent study, higher consumption of water (ml)/kg per weight was negatively associated with BMI, body fat, waist circumference, insulin levels, HOMA-IR, and positively with HDL cholesterol in children. In addition, overweight and obese children drank less water (ml)/kg per weight than normal weight ones [15].

Results also showed significantly increased OxLDL levels in daily consumers of chocolate drinks. In contrast, Khan et al. [16] found that regular consumption of cocoa powder with milk reduces oxidized LDL levels in subjects at high risk of cardiovascular disease. A possible explanation for this contradictory finding is that it concerns different study populations and that the chocolate drinks drank by children in this study are not only made of cocoa powder and milk but probably contain a higher amount of sugar and fat.

Moreover, “high-fat diet” (HFD) and “always eating a dessert at the end of the meal” were correlated with increased serum oxLDL levels with a trend towards significance.

Kesh et al. [17] elucidated the mechanistic links between HFD-induced oxidative stress and its impact on metabolic complications development. However, in our study, we were not able to prove a significant association between a “high-fat diet” and increased oxLDL levels. This might be due to our study population. The effects of HFD might only become apparent over a longer time and since we focused on children, the effects may not have been apparent yet. Since it does show a trend towards significance, this might also be due to the small sample size. Therefore, expanding sampling is mandatory.

In a study by Jung et al. [18], the second factor, “always eating a dessert at the end of the meal”, was significantly inversely associated with fluorescent oxidation products, a global index of oxidative stress. In our study, this association could not be proven significant. Considering that most desserts are high in sugar and fat and that consuming chocolate drinks every day for breakfast was significantly associated with serum oxLDL levels in this study, we expected to see a significant association between eating desserts and oxLDL levels. Again, this could be due to our small sample size and expanding the sample might reveal a significant association between both factors.

On the contrary, we found significantly decreased oxLDL levels in subjects consuming a breakfast based mainly on fruits. Holt et al. [19] described the beneficial effects of fruit and vegetable intake on markers of inflammation and oxidative stress in adolescents. A variety of fruits and vegetables contain folate and antioxidants, such as vitamin C and beta-carotene. These micronutrients have been related to lower levels of markers of inflammation and oxidative stress. These findings provide support for the dietary guideline to consume five or more servings a day of fruits and vegetables to promote health.

Although our results are consistent with findings suggesting that dietary choices and physical activity may not have an immediate impact on OS response in children with overweight and obesity, unhealthy eating pattern, in particular increased fat and sugar consumption and poor water intake, might be considered as external exposome predictors of OS, that need to be measured repeatedly in certain important life stages, as growth, to improve health status by predicting and preventing disease.