Cardiology in the Young 2015; Page 1 of 6
© Cambridge University Press, 2015
doi:10.1017/S1047951115000050
Original Article Breakfast frequency, adiposity, and cardiovascular risk factors as markers in adolescents Suziane U. Cayres,1,2 Ismael F. F. Júnior,1,3 Maurício F. Barbosa,4 Diego G. D. Christofaro,1,2 Rômulo A. Fernandes1,2 Post-Graduate Program in Movement Sciences, Sao Paulo State University – UNESP, Rio Claro; 2Laboratory of Investigation in Exercise – LIVE; 3Department of Physical Education, Sao Paulo State University – UNESP, Presidente Prudente; 4Program of Post-Graduate in Radiology, Federal University of Sao Paulo – UNIFESP, Brazil 1
Abstract Objective: To analyse the relationship between skipping breakfast and haemodynamic, metabolic, inflammatory, and cardiovascular risk factors in adolescents. Methods: A cross-sectional study was carried out with information from an ongoing cohort study in Presidente Prudente, São Paulo, Brazil. The sample comprised of 120 adolescents (11.7 ± 0.8 years old) who met the following inclusion criteria: age between 11 and 14 years; enrolled in the school unit of elementary education; absence of any known disease; and no drug consumption. The parents or legal guardians of the patients signed a formal informed consent. Skipping breakfast was self-reported through face-to-face interviews. Blood pressure, intima-media thickness, trunk fatness, total and fractional cholesterol levels – high-density lipoprotein cholesterol and low-density lipoprotein cholesterol – triacylglycerol levels, and high-sensitivity C-reactive protein levels were measured. Results: In this study, 47.5% (95% CI: 38.5–56.4%) of the adolescents reported skipping breakfast at least 1 day/week. Adolescents who skipped breakfast had higher values of trunk fatness and systolic blood pressure. Breakfast frequency was negatively related to systolic blood pressure (β −1.99 [ − 3.67; −0.31]) and z score dyslipidaemia (β −0.46 [ − 0.90; −0.01]), but this relationship was mediated by trunk fatness. Conclusion: Skipping breakfast is related to cardiovascular risk factors in adolescents, and this relationship was mainly mediated by trunk fatness. Keywords: Adolescent; cardiovascular risk factors; skipping breakfast Received: 28 November 2014; Accepted: 11 January 2015
N RECENT YEARS, SEVERAL RISK BEHAVIOURS HAVE
I
been widely linked with the establishment/ development of chronic diseases in paediatric and adult populations – for example, sedentary lifestyle, smoking, and consumption of fast foods.1 More recently, researchers have focussed their efforts on understanding the effects of non-traditional risk behaviours over health outcomes. With this in mind, recent studies have analysed the relationship between skipping meals and unhealthy outcomes.2–5 More specifically, skipping breakfast has been pointed out Correspondence to: S. U. Cayres, MSc, Department of Physical Education, Roberto Simonsen Street, 305, Presidente Prudente, 19060900 Sao Paulo, Brazil. Tel: + 183 229 5400; Fax: (18) 3221-4391; E-mail: [email protected]
as a potentially harmful behaviour, as it is related to increased body fatness in paediatric populations.3–5 Among men, follow-up data have supported a significant relationship between higher breakfast frequency and lower development of CHDs, which is apparently mediated by the effect of obesity, diabetes mellitus, arterial hypertension, and hypercholesterolaemia.6 In agreement with this, previous investigations have identified that, in obese adolescents, skipping breakfast is related to an unfavourable lipid profile and increased fasting glucose levels.2 On the other hand, although significantly linked to the above-mentioned outcomes, there is an absence of data analysing the effect of skipping breakfast on cardiovascular and inflammatory outcomes in paediatric populations.
2
Cardiology in the Young
Thus, our objective was to analyse the relationship between frequency of breakfast consumption and metabolic, inflammatory, and cardiovascular risk factors in adolescents.
Methods Sample The present study is made up of baseline measures from a cohort study, which was being carried out in Presidente Prudente city (200,000 inhabitants; western Sao Paulo State, Brazil) during 2013 and 2014 (second half). Initially, a minimum sample size was estimated (r = 0.26, 80% of power and α of 5%),7 which identified that at least 86 adolescents should be recruited. In all, seven large public and primary schools in the metropolitan region of the city were invited to participate in the study, and, of these, three agreed to participate. Subsequently, all school children between 11 and 14 years of age from the included schools (overall students n = 495) were invited to participate in the study, and 120 adolescents agreed to participate and fulfilled all the inclusion criteria; age between 11 and 14 years; regularly enrolled in the school unit; absence of any known diseases (healthy patient apparently); not consuming drugs; and signature of parents or legal guardians. The study had been previously approved by the Human Research Ethics Committee (process: 322.650/2013) of the Universidade Estadual Paulista, Presidente Prudente, Brazil. Biochemical variables Blood samples were collected in the morning, after 12 hours of overnight fasting, by a nurse in a private laboratory, which met all the quality control standards adopted by the Brazilian Health Ministry. Total cholesterol, its fractions – high-density lipoprotein cholesterol and low-density lipoprotein cholesterol – and triacylglycerol levels were measured using an enzymatic colorimetric kit processed in an Autohumalyzer (Dimension RxL Max model; Siemens Dade-Behring, Deerfield, Illinois). High-sensitivity C-reactive protein level was determined by turbidimetric method (model LabMax 240; LABEST brand, Chema Diagnostica, Monsano, Italy) using an enzyme kit (Millipore, St. Charles, Missouri, United States of America; intraand inter-assay coefficients ranging between 4.6 and 6.0 kit %, respectively). A continuous score was computed from the four lipid variables. Each lipid variable was standardised ([value − mean]/standard deviation [high-density lipoprotein cholesterol z scores were multiplied by −1]). The z scores of the individual factors were then summed to create the cluster lipid variable, identified as dyslipidaemia.
2015
Blood pressure Systolic and diastolic blood pressure were assessed using the oscillometric method in an automatic device (model HEM 742 INT; Omron Healthcare Inc. Intellisense, Bannockburn, Illinois, United States of America), validated by Christofaro et al.8 All measurements were performed after 10 minutes at rest in the seated position. A cuff, of appropriate size for the arm circumference age below 13 years [child size] (6 × 12 cm) and age above 13 years [medium size] (9 × 18 cm), was wrapped around the midpoint of the humerus of the right arm. Adjustments were made where necessary for obese adolescents with an arm circumference greater than that of their age group. Measurements were taken three times, separated by an interval of one minute, and the average of the last two measurements was considered as the blood pressure.9 Intima-media thickness The carotid intima-media thickness and femoral intima-media thickness were assessed by a trained doctor using a Doppler ultrasound examination (model Philips HD 11 XE; Philips, Barueri, Sao Paulo, Brazil), equipped with a high resolution, multi-frequency linear transducer, set to 12 MHz, in a private hospital in the city. All recommendations of the Brazilian Society of Cardiology10 were adopted for this procedure. The common carotid artery and the femoral artery (right side) were evaluated in order to estimate intima-media thickness; in others words, the distance between two echogenic lines that show the lumen/intima interface and media/adventitia of the arterial wall was evaluated.11 When testing the common carotid artery, the neck was slightly hyperextended and inclined at an angle of 45°. To assess the femoral artery, the adolescent’s leg was stretched out on the bed and the measurement was carried out near the inguinal line. Trunk fatness Trunk fatness was assessed using a dual-energy X-ray absorptiometry scanner (Lunar DPX-NT; General Electric Healthcare, Little Chalfont, Buckinghamshire, United Kingdom) with GE Medical System Lunar software, version 4.7, and this variable was expressed as a percentage. The scanner quality was tested by a trained researcher before each measurement, in accordance with the manufacturer’s recommendations. Following this stage, an examination of the entire body was performed. Throughout the test, the patients wore light clothing, no shoes, and remained in the supine position on the machine, remaining immobile for ~15 minutes.
Cayres et al: Breakfast intake and cardiovascular risk factors
Breakfast frequency Breakfast frequency was assessed through face-to-face interviews. Taking into account a typical week, the number of days with breakfast consumption was reported by the adolescent (variable ranging from zero to seven days). Skipping breakfast denoted a breakfast frequency of ⩽6 days/week. Other information Concurrent with the face-to-face interview, ethnicity – white, black, oriental, and other – sex, and chronological age were established. In addition, body weight was measured using an electronic scale (Filizzola PL 150model; Filizzola Ltda, Sao Paulo, Brazil), and height was measured using a wall-mounted stadiometer (Sanny model; American Medical of the Brazil Ltda, Brazil). All anthropometric measurements were performed according to standardised techniques. Statistical analyses First, normality of the data set was assessed and nonparametric variables were transformed to logarithm (high sensitivity C-reactive protein). Descriptive statistics were composed of mean values and their standard deviations. One-way analysis of variance (Tukey’s post-hoc) and the Student t test were used to compare numerical variables. The Spearman correlation (rho) was applied to analyse the relationship between breakfast intake frequency (low and high) and the dependent variables (systolic blood pressure,
3
diastolic blood pressure, total cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, triacylglycerol, dyslipidaemia, carotid intimamedia thickness, femoral intima-media thickness, and high-sensitivity C-reactive protein). Variables with significant relationships were included in the multivariate model (linear regression), composed of breakfast intake and dependent variables (crude model); adjusted by sex (Model 2); sex, age, and ethnicity (Model 3); and sex, age, ethnicity, and trunk fatness (Model 4). Statistical significance was set at 5% (p-value < 0.05), and all statistical analyses were performed using BioEstat software (version 5.0, Tefé, Amazonas).
Results The overall sample comprised of 120 adolescents of both the sexes (62 boys [mean age 11.7 ± 0.8 years]). In this study, 47.5% (95% CI: 38.5–56.4%) of the adolescents (n = 57) reported skipping breakfast at least 1 day/week. Adolescents who skipped breakfast had higher values of trunk fatness (p-value = 0.002) and systolic blood pressure (p-value = 0.040) (Table 1). Adolescents with a higher frequency of breakfast consumption had lower values of trunk fatness (None: 37.7 [CI = 33.3–42.1]; 1–2 days: 35.7 [CI = 27.4–44.1]; 3–5 days: 32.6 [CI = 28.1–37.1]; 6–7 days: 29.1 [CI = 26.2–31.9]; one-way analysis of variance with p-value = 0.008, and Tukey’s post-hoc with p-value = 0.006 for the comparison between the groups “None” and “6–7 days”).
Table 1. General characteristics of the adolescents according to skipping breakfast (Presidente Prudente, Sao Paulo, Brazil, 2013). Skipping breakfast Variables
At least 1 day/week (n = 57) Mean (SD)
Never (n = 63) Mean (SD)
p-value
Age (years) Weight (kg) Height (cm) BMI (kg/m2) TF (%) TC (mg/dl) HDL-c (mg/dl) LDL-c (mg/dl) TG (mg/dl) hsCRP (mg/dl)# SBP (mmHg) DBP (mmHg) CMIT (mm) FIMT (mm)
11.7 (0.84) 54.3 (11.9) 155.9 (7.6) 20.6 (4.4) 35.5 (10.8) 163.1 (28.9) 49.7 (11.7) 95.5 (23.1) 83.9 (40.1) − 0.22 (0.5) 113.6 (10.6) 69.7 (10.3) 0.46 (0.04) 0.39 (0.05)
11.7 (0.6) 50.2 (13.0) 155.2 (6.4) 22.2 (3.8) 29.1 (11.4) 161.6 (21.1) 50.4 (10.5) 94.9 (18.6) 81.1 (36.9) − 0.21 (0.6) 109.5 (10.9) 67.1 (10.8) 0.45 (0.03) 0.38 (0.09)
0.676 0.147 0.667 0.104 0.002* 0.740 0.723 0.862 0.694 0.965 0.040* 0.164 0.795 0.388
Variable under logarithm transformation; BMI = body mass index; CIMT = carotid intima-media thickness; DBP = diastolic blood pressure; FIMT = femoral intima-media thickness; HDL-c = high-density lipoprotein cholesterol; hsCRP = high-sensitivity C-reactive protein; LDL-c = low-density lipoprotein cholesterol; SBP = systolic blood pressure; TC = total cholesterol; TF = trunk fatness; TG = triacylglycerol; SD = standard deviation *p-value
© Cambridge University Press, 2015
doi:10.1017/S1047951115000050
Original Article Breakfast frequency, adiposity, and cardiovascular risk factors as markers in adolescents Suziane U. Cayres,1,2 Ismael F. F. Júnior,1,3 Maurício F. Barbosa,4 Diego G. D. Christofaro,1,2 Rômulo A. Fernandes1,2 Post-Graduate Program in Movement Sciences, Sao Paulo State University – UNESP, Rio Claro; 2Laboratory of Investigation in Exercise – LIVE; 3Department of Physical Education, Sao Paulo State University – UNESP, Presidente Prudente; 4Program of Post-Graduate in Radiology, Federal University of Sao Paulo – UNIFESP, Brazil 1
Abstract Objective: To analyse the relationship between skipping breakfast and haemodynamic, metabolic, inflammatory, and cardiovascular risk factors in adolescents. Methods: A cross-sectional study was carried out with information from an ongoing cohort study in Presidente Prudente, São Paulo, Brazil. The sample comprised of 120 adolescents (11.7 ± 0.8 years old) who met the following inclusion criteria: age between 11 and 14 years; enrolled in the school unit of elementary education; absence of any known disease; and no drug consumption. The parents or legal guardians of the patients signed a formal informed consent. Skipping breakfast was self-reported through face-to-face interviews. Blood pressure, intima-media thickness, trunk fatness, total and fractional cholesterol levels – high-density lipoprotein cholesterol and low-density lipoprotein cholesterol – triacylglycerol levels, and high-sensitivity C-reactive protein levels were measured. Results: In this study, 47.5% (95% CI: 38.5–56.4%) of the adolescents reported skipping breakfast at least 1 day/week. Adolescents who skipped breakfast had higher values of trunk fatness and systolic blood pressure. Breakfast frequency was negatively related to systolic blood pressure (β −1.99 [ − 3.67; −0.31]) and z score dyslipidaemia (β −0.46 [ − 0.90; −0.01]), but this relationship was mediated by trunk fatness. Conclusion: Skipping breakfast is related to cardiovascular risk factors in adolescents, and this relationship was mainly mediated by trunk fatness. Keywords: Adolescent; cardiovascular risk factors; skipping breakfast Received: 28 November 2014; Accepted: 11 January 2015
N RECENT YEARS, SEVERAL RISK BEHAVIOURS HAVE
I
been widely linked with the establishment/ development of chronic diseases in paediatric and adult populations – for example, sedentary lifestyle, smoking, and consumption of fast foods.1 More recently, researchers have focussed their efforts on understanding the effects of non-traditional risk behaviours over health outcomes. With this in mind, recent studies have analysed the relationship between skipping meals and unhealthy outcomes.2–5 More specifically, skipping breakfast has been pointed out Correspondence to: S. U. Cayres, MSc, Department of Physical Education, Roberto Simonsen Street, 305, Presidente Prudente, 19060900 Sao Paulo, Brazil. Tel: + 183 229 5400; Fax: (18) 3221-4391; E-mail: [email protected]
as a potentially harmful behaviour, as it is related to increased body fatness in paediatric populations.3–5 Among men, follow-up data have supported a significant relationship between higher breakfast frequency and lower development of CHDs, which is apparently mediated by the effect of obesity, diabetes mellitus, arterial hypertension, and hypercholesterolaemia.6 In agreement with this, previous investigations have identified that, in obese adolescents, skipping breakfast is related to an unfavourable lipid profile and increased fasting glucose levels.2 On the other hand, although significantly linked to the above-mentioned outcomes, there is an absence of data analysing the effect of skipping breakfast on cardiovascular and inflammatory outcomes in paediatric populations.
2
Cardiology in the Young
Thus, our objective was to analyse the relationship between frequency of breakfast consumption and metabolic, inflammatory, and cardiovascular risk factors in adolescents.
Methods Sample The present study is made up of baseline measures from a cohort study, which was being carried out in Presidente Prudente city (200,000 inhabitants; western Sao Paulo State, Brazil) during 2013 and 2014 (second half). Initially, a minimum sample size was estimated (r = 0.26, 80% of power and α of 5%),7 which identified that at least 86 adolescents should be recruited. In all, seven large public and primary schools in the metropolitan region of the city were invited to participate in the study, and, of these, three agreed to participate. Subsequently, all school children between 11 and 14 years of age from the included schools (overall students n = 495) were invited to participate in the study, and 120 adolescents agreed to participate and fulfilled all the inclusion criteria; age between 11 and 14 years; regularly enrolled in the school unit; absence of any known diseases (healthy patient apparently); not consuming drugs; and signature of parents or legal guardians. The study had been previously approved by the Human Research Ethics Committee (process: 322.650/2013) of the Universidade Estadual Paulista, Presidente Prudente, Brazil. Biochemical variables Blood samples were collected in the morning, after 12 hours of overnight fasting, by a nurse in a private laboratory, which met all the quality control standards adopted by the Brazilian Health Ministry. Total cholesterol, its fractions – high-density lipoprotein cholesterol and low-density lipoprotein cholesterol – and triacylglycerol levels were measured using an enzymatic colorimetric kit processed in an Autohumalyzer (Dimension RxL Max model; Siemens Dade-Behring, Deerfield, Illinois). High-sensitivity C-reactive protein level was determined by turbidimetric method (model LabMax 240; LABEST brand, Chema Diagnostica, Monsano, Italy) using an enzyme kit (Millipore, St. Charles, Missouri, United States of America; intraand inter-assay coefficients ranging between 4.6 and 6.0 kit %, respectively). A continuous score was computed from the four lipid variables. Each lipid variable was standardised ([value − mean]/standard deviation [high-density lipoprotein cholesterol z scores were multiplied by −1]). The z scores of the individual factors were then summed to create the cluster lipid variable, identified as dyslipidaemia.
2015
Blood pressure Systolic and diastolic blood pressure were assessed using the oscillometric method in an automatic device (model HEM 742 INT; Omron Healthcare Inc. Intellisense, Bannockburn, Illinois, United States of America), validated by Christofaro et al.8 All measurements were performed after 10 minutes at rest in the seated position. A cuff, of appropriate size for the arm circumference age below 13 years [child size] (6 × 12 cm) and age above 13 years [medium size] (9 × 18 cm), was wrapped around the midpoint of the humerus of the right arm. Adjustments were made where necessary for obese adolescents with an arm circumference greater than that of their age group. Measurements were taken three times, separated by an interval of one minute, and the average of the last two measurements was considered as the blood pressure.9 Intima-media thickness The carotid intima-media thickness and femoral intima-media thickness were assessed by a trained doctor using a Doppler ultrasound examination (model Philips HD 11 XE; Philips, Barueri, Sao Paulo, Brazil), equipped with a high resolution, multi-frequency linear transducer, set to 12 MHz, in a private hospital in the city. All recommendations of the Brazilian Society of Cardiology10 were adopted for this procedure. The common carotid artery and the femoral artery (right side) were evaluated in order to estimate intima-media thickness; in others words, the distance between two echogenic lines that show the lumen/intima interface and media/adventitia of the arterial wall was evaluated.11 When testing the common carotid artery, the neck was slightly hyperextended and inclined at an angle of 45°. To assess the femoral artery, the adolescent’s leg was stretched out on the bed and the measurement was carried out near the inguinal line. Trunk fatness Trunk fatness was assessed using a dual-energy X-ray absorptiometry scanner (Lunar DPX-NT; General Electric Healthcare, Little Chalfont, Buckinghamshire, United Kingdom) with GE Medical System Lunar software, version 4.7, and this variable was expressed as a percentage. The scanner quality was tested by a trained researcher before each measurement, in accordance with the manufacturer’s recommendations. Following this stage, an examination of the entire body was performed. Throughout the test, the patients wore light clothing, no shoes, and remained in the supine position on the machine, remaining immobile for ~15 minutes.
Cayres et al: Breakfast intake and cardiovascular risk factors
Breakfast frequency Breakfast frequency was assessed through face-to-face interviews. Taking into account a typical week, the number of days with breakfast consumption was reported by the adolescent (variable ranging from zero to seven days). Skipping breakfast denoted a breakfast frequency of ⩽6 days/week. Other information Concurrent with the face-to-face interview, ethnicity – white, black, oriental, and other – sex, and chronological age were established. In addition, body weight was measured using an electronic scale (Filizzola PL 150model; Filizzola Ltda, Sao Paulo, Brazil), and height was measured using a wall-mounted stadiometer (Sanny model; American Medical of the Brazil Ltda, Brazil). All anthropometric measurements were performed according to standardised techniques. Statistical analyses First, normality of the data set was assessed and nonparametric variables were transformed to logarithm (high sensitivity C-reactive protein). Descriptive statistics were composed of mean values and their standard deviations. One-way analysis of variance (Tukey’s post-hoc) and the Student t test were used to compare numerical variables. The Spearman correlation (rho) was applied to analyse the relationship between breakfast intake frequency (low and high) and the dependent variables (systolic blood pressure,
3
diastolic blood pressure, total cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, triacylglycerol, dyslipidaemia, carotid intimamedia thickness, femoral intima-media thickness, and high-sensitivity C-reactive protein). Variables with significant relationships were included in the multivariate model (linear regression), composed of breakfast intake and dependent variables (crude model); adjusted by sex (Model 2); sex, age, and ethnicity (Model 3); and sex, age, ethnicity, and trunk fatness (Model 4). Statistical significance was set at 5% (p-value < 0.05), and all statistical analyses were performed using BioEstat software (version 5.0, Tefé, Amazonas).
Results The overall sample comprised of 120 adolescents of both the sexes (62 boys [mean age 11.7 ± 0.8 years]). In this study, 47.5% (95% CI: 38.5–56.4%) of the adolescents (n = 57) reported skipping breakfast at least 1 day/week. Adolescents who skipped breakfast had higher values of trunk fatness (p-value = 0.002) and systolic blood pressure (p-value = 0.040) (Table 1). Adolescents with a higher frequency of breakfast consumption had lower values of trunk fatness (None: 37.7 [CI = 33.3–42.1]; 1–2 days: 35.7 [CI = 27.4–44.1]; 3–5 days: 32.6 [CI = 28.1–37.1]; 6–7 days: 29.1 [CI = 26.2–31.9]; one-way analysis of variance with p-value = 0.008, and Tukey’s post-hoc with p-value = 0.006 for the comparison between the groups “None” and “6–7 days”).
Table 1. General characteristics of the adolescents according to skipping breakfast (Presidente Prudente, Sao Paulo, Brazil, 2013). Skipping breakfast Variables
At least 1 day/week (n = 57) Mean (SD)
Never (n = 63) Mean (SD)
p-value
Age (years) Weight (kg) Height (cm) BMI (kg/m2) TF (%) TC (mg/dl) HDL-c (mg/dl) LDL-c (mg/dl) TG (mg/dl) hsCRP (mg/dl)# SBP (mmHg) DBP (mmHg) CMIT (mm) FIMT (mm)
11.7 (0.84) 54.3 (11.9) 155.9 (7.6) 20.6 (4.4) 35.5 (10.8) 163.1 (28.9) 49.7 (11.7) 95.5 (23.1) 83.9 (40.1) − 0.22 (0.5) 113.6 (10.6) 69.7 (10.3) 0.46 (0.04) 0.39 (0.05)
11.7 (0.6) 50.2 (13.0) 155.2 (6.4) 22.2 (3.8) 29.1 (11.4) 161.6 (21.1) 50.4 (10.5) 94.9 (18.6) 81.1 (36.9) − 0.21 (0.6) 109.5 (10.9) 67.1 (10.8) 0.45 (0.03) 0.38 (0.09)
0.676 0.147 0.667 0.104 0.002* 0.740 0.723 0.862 0.694 0.965 0.040* 0.164 0.795 0.388
Variable under logarithm transformation; BMI = body mass index; CIMT = carotid intima-media thickness; DBP = diastolic blood pressure; FIMT = femoral intima-media thickness; HDL-c = high-density lipoprotein cholesterol; hsCRP = high-sensitivity C-reactive protein; LDL-c = low-density lipoprotein cholesterol; SBP = systolic blood pressure; TC = total cholesterol; TF = trunk fatness; TG = triacylglycerol; SD = standard deviation *p-value
