Abstract
Abstract
Objective:
To examine the potential association between exclusive breastfeeding and its duration on physical fitness (PF) components during childhood.
Materials and Methods:
A random sample of 5,125 dyads children and their mothers was evaluated. With the use of a standardized questionnaire, telephone interviews were carried out for the collection of maternal lifestyle factors (e.g., breastfeeding and its duration, etc.). Data from five PF tests (e.g., vertical jump, standing long jump, small ball throw, 30-m sprint, and 20-m shuttle run) were used to assess lower and upper body strength, speed, and cardiorespiratory fitness (CRF). Linear and logistic regression models were estimated and adjusted for children's body mass index (BMI) and birth weight, and parental factors (prepregnancy BMI, gestational weight gain, gestational age, pregnancy in vitro, parity before, and educational level).
Results:
Among boys, exclusive breastfeeding was favorably associated with CRF (b = 0.07), lower body strength (b = 0.41), upper body strength (b = 0.10), and speed (b = −0.11). Also, among girls, we found a favorable association between exclusive breastfeeding and CRF (b = 0.07), lower body strength (b = 0.47), upper body strength (b = 0.10), and speed (b = −0.11). All of the associations remained significant after adjusting for several potential confounders. With the exception of speed test in girls, children who were exclusively breastfed ≥6 months had 10–40% increased odds for average/high performances in PF tests in comparison with those who were breastfed <1 month.
Conclusions:
Exclusive breastfeeding ≥6 months had a favorable influence on PF test performances in childhood. It seems that exclusive breastfeeding could play a significant role in children's future health.
Introduction
Physical fitness (PF) is defined as the “ability to carry out daily tasks with vigor and alertness, without undue fatigue and with ample energy to enjoy leisure-time pursuits and to meet unforeseen emergencies.” 1 As PF is a powerful marker of cardiovascular health in children, it is considered that a sufficient level of PF in childhood is needed to carry forward favorable behavioral and biological effects into later life. 2 Epidemiologic findings have proposed that improvement in PF is associated with a healthier life in children, in a dose–response fashion. 3 On the contrary, low levels of PF in children are related to numerous risk factors such as hyperlipidemia, hypertension, and obesity. 3 Moreover, a meta-analysis has shown that the relative risk for cardiovascular disease was higher among those who were below the 25th percentile of the PF distribution compared with those in higher percentiles. 4 PF is influenced by numerous factors such as biological, genetic, environmental and lifestyle factors, as well as breastfeeding.3–7
According to the World Health Organization, breastfeeding is the natural approach of providing infants with the needed nutrients for healthy growth and development. 8 Specifically, exclusive breastfeeding is recommended for the first 6 months of life, followed by sustained breastfeeding for the first year of life and longer. 9 Numerous international organizations have been paying attention towards enhancing the initiation, continuance, and exclusivity of breastfeeding. 10 Exclusive breastfeeding is influenced by a complex of factors such as psychological, sociocultural, demographics, biomedical, health care system, and social support.11–13 Among the potential risk factors for avoiding exclusive breastfeeding are maternal age and obesity status, maternal education, excessive gestational weight gain (GWG), parity before, nationality, infant characteristics, etc.12,13 The favorable effects of breastfeeding on infant health include protection against common diseases and cardiovascular disease risk factors such as obesity, hypertension, and diabetes mellitus during childhood, neuropsychological benefits, enhanced motor development, etc.14–19 Moreover, it has been proposed that human milk components, such as polyunsaturated fatty acids, adipokines, and prostaglandin J2, could explain the beneficial effects of breastfeeding on cardiorespiratory fitness (CRF). 20
However, to the best of our knowledge, few studies have examined the potential effect of exclusive breastfeeding and its duration on PF in children, while most of them have focused only on the effect of breastfeeding on CRF.21–24 Specifically, two studies have proposed that a longer period of exclusive breastfeeding is associated with a favorable effect on CRF in children.21,22 On the contrary, other researchers could not confirm the previous findings since they did not find a significant association between breastfeeding duration and CRF in children.23,24 Furthermore, results from a study among European adolescents have shown that longer breastfeeding is connected with better lower body explosive strength. 24
From the public health aspect, because early infant feeding practices are possibly modifiable, it is essential to better understand the potential programming effect of breastfeeding on PF. This information could further support the development of health interventions to increase exclusive breastfeeding.
Thus, we aimed to examine the effects of exclusive breastfeeding and its duration on PF components such as CRF, muscular strength of upper and lower body, speed, and agility in a large, representative cohort of Greek children 8–9 years old, taking into consideration several potential confounders.
Materials and Methods
Study design
Population-based data were derived from 10 national school-based health surveys, following an official request to the Greek Ministry of Education. The national database included anthropometric data and information on age, gender, city and area, home address, and telephone number, which were collected yearly during the specific time period (spring) from 1997 to 2007, with the exception of 2002, in almost all schools of primary education (roughly 85%); schools that did not participate were from borderland areas, with small numbers of children. Thus, from 1997 to 2007, a total of 651,582 eight- to nine-year-old children (51% boys and 49% girls, over 95% of the total student population) participated in the study. Measurements were performed by two trained physical education (PE) teachers in each school. PE teachers followed a specific protocol taught to them during corresponding seminars held by the Greek General Secretariat of Sports. The same protocol was employed in all schools.
Data extraction
A sample of 5,500 children (0.8% of the entire population) was randomly extracted from the database and their mothers were contacted via telephone. Random extraction was performed using a statistical software. The number of 5,500 subjects was adequate to achieve statistical power ≥99% for evaluating a 0.10 ± 0.05 change in regression coefficients at 5% significance level of two-sided tested hypotheses. The random sampling was stratified based on the region and place of living (e.g., rural/urban), according to the National Statistical Agency and equally distributed during the study period (i.e., 500 mothers per year). The women who refused to participate in the study were 183 (3.3%). The sample of mother–child dyads covered all geographical regions of Greece (e.g., mainland Greece and the islands). The information of the proposed protocol was collected through telephone interviews based on the computer-aided telephone interview method. To validate the process, 100 face-to-face interviews were conducted to check for discrepancies with the information collected via telephone. No such discrepancies were noted in any of the variables evaluated.
Measurements
All the necessary information was collected using a standardized questionnaire, named the Childhood Obesity Pregnancy Determinants (ChOPreD) questionnaire, designed and developed with collaboration of the Harokopio University Department of Nutrition and Dietetics and Department of Geography, and the University of Texas Medical Branch Department of Internal Medicine. The ChOPreD questionnaire was tested and internally revised by study investigators during a pilot study, which confirmed its construct validity. During data collection, the mothers were asked to provide information contained in their pregnancy ultrasound records (e.g., body weight) and recall certain information (e.g., exercise levels, smoking patterns, and alcohol consumption). Mothers in Greece have ultrasounds at the start of pregnancy and several times during its progress and receive records of the results. Only mothers who had full set of records were included in the study, which finalized the sample of 5,125 mother–children dyads. Data recall relating to the perinatal period is very common in pregnancy-related studies. Also, recall of breastfeeding practice is considered a valid and reliable estimate. 25
The body mass index (BMI) data of the children at the age of 8 years was calculated based on the data retrieved from the national database. The BMI status of the offspring at the age of 8 years and in the early adulthood was determined based on cut-off points suggested by the International Obesity Task Force. 26
GWG was calculated based on the difference between the mother's weight at the last and first visits based on ultrasound records. Each mother was categorized according to the Institute of Medicine (IOM) guidelines: (1) for mothers who were underweight at the start of pregnancy, adequate GWG was 12.5–18 kg; (2) for normal-weight mothers at the start of pregnancy, adequate GWG was 11.5–16 kg; (3) for mothers who were overweight at the start of pregnancy, adequate GWG was 7–11.5 kg; and (4) for mothers who were obese at the start of pregnancy, adequate GWG was 5–9 kg. Mothers who gained more or less weight than beyond these ranges were categorized as IOM-excess or -inadequate, respectively. For the purposes of the current study, physical activity is defined as any form of bodily movement produced by skeletal muscles that increases energy expenditure over the level of physical rest, thereby offering numerous benefits to the human body. This can include a wide range of activities, such as leisure activities, participation in organized sports, exercise, physical work, etc. 27
Fitness tests
Five fitness tests were administered by two trained PE professionals in each school: (1) vertical jump (VJ; jump from a squatting position at the start); (2) standing long jump (SLJ; jump as far as possible from a standing position at the start). Both these tests assess lower body explosive power. Also administered were: (3) small ball throw (SBT; 1 kg with both hands in a standing position), to assess upper body explosive strength; (4) 30-m sprint (30mS; from a standing start), to evaluate speed and agility; and (5) multistage 20-m shuttle run (20mSRT), to estimate CRF. The 20mSRT test consists of measuring the number of laps completed by subjects running up and down between two lines, set 20 m apart, at an initial speed of 8.5 km/hour, which increases by 0.5 km/hour every minute, using a prerecorded audio tape. The above widely used five fitness tests were selected as being representative of explosive, anaerobic, and aerobic performance. Repeat tests (two trials) were allowed for the VJ, SLJ, SBT, and 30mS, with the best performance of each recorded. Students' performance in PF tests was evaluated based on the PF normative age- and sex-specific values for 8- to 10-year-old Greek boys and girls. 28 Particularly, for each of the five PF tests applied, a performance ≤25th percentile was considered as low; between the 25th and 75th, as average; and ≥75th, as high. Using the abovementioned classification, a combined variable representing total poor PF was constructed, defined as the combined low performance (≤25th percentile) in all five PF tests applied.
Breastfeeding
Mothers were asked if they had breastfed their offspring and, if so, what the duration was (in months) of (1) exclusive breastfeeding and (2) overall breastfeeding. Breastfeeding is a special practice for most mothers, so they can easily recall details about it.
Study approval
The study was approved by the Bioethics Committee of Harokopio University. Oral approval was obtained from all mothers who agreed to participate in the study, and written informed consent was obtained from those participants who took part in the validation process of the study.
Statistical analysis
Continuous variables were presented as mean ± standard deviation given that they were normally distributed (as examined by the use of histograms and P–P plots). Categorical variables were presented as frequencies. The chi-square test evaluated associations between categorical variables, and the Student's t test was applied to evaluate differences in mean values of normally distributed variables. To assess the relationships between exclusive breastfeeding (as a continuous variable) and PF test performances, we applied linear regression analysis in an extended model approach. Model 1 included only the predictor (exclusive breastfeeding) and the dependent variable (e.g., aerobic fitness). For model 2, a set of confounders (i.e., children's BMI and low birth weight) was added into the model. For model 3, prepregnancy BMI status and GWG also were added into the model. Finally, for model 4, gestational age, pregnancy in vitro, parity before, and educational level were added into the model. Before that, every possible effect modification between the proposed risk factors and the confounders was examined, but all interaction terms were not statistical significant (p > 0.05). Furthermore, aiming to assess the potential effect of exclusive breastfeeding and its duration (<1 versus ≥6 months) on PF test performance (low versus high/average), logistic regression analysis was implemented and odds ratio with the corresponding 95% confidence interval (CI) were calculated. The Hosmer and Lemeshow's goodness-of-fit test was calculated to evaluate the model's goodness-of-fit, and residual analysis was implicated using the dbeta, the leverage, and Cook's distance D statistics to identify outliers and influential observations. All analyses were performed using SPSS version 23.0 for Windows (SPSS, Inc., Chicago, IL). Statistical significance level from two-sided hypotheses was set at 5% level (p ≤ 0.05).
Results
Mothers who did not have full set of data were 192 (3.5%), while those who did not participate in the study were 183 (3.3%). Table 1 presents parental and offspring characteristics of the study sample. In the current study, percentages of mothers who had breastfed or had exclusively breastfed their offspring for ≥6 months were 22.4% and 15.2%, respectively. Table 2 presents demographic, PF, and clinical characteristics of children and their mothers by exclusive breastfeeding duration (e.g., <1, 1–5, and ≥6 months) and sex. The performances in all PF tests were higher in those who were exclusively breastfed ≥6 months compared with those who were exclusively breastfed <1 month, in both sexes. Less obese mothers at first visit had exclusively breastfed ≥6 months than normal-weight ones (p < 0.001), while more mothers who had excess weight gain during pregnancy had exclusively breastfed their offspring compared with those who had adequate weight gain (p = 0.006).
Characteristics (Mean ± Standard Deviation or Percentages) of the Study Sample of Parents and Their Offspring
BMI, body mass index; GWG, gestational weight gain; IOM, Institute of Medicine.
Demographic and Clinical Characteristics of Child and Mother by Exclusive Breastfeeding Duration and Sex
P < 0.05.
Table 3 presents linear regression models showing the estimated change in mean performances in PF tests per month increase in exclusive breastfeeding, by sex. In unadjusted analysis, exclusive breastfeeding was positively associated with all PF components (all p-values <0.001), in both sexes. For example, the analysis showed that increase per 1 month in exclusive breastfeeding was associated with an increase of 0.10 stage in 20-mSRT (95% CI 0.08–0.12) among boys and girls. This association remained significant after controlling for children's BMI and low birth weight (model 2) and also after additional controlling for prepregnancy BMI status and GWG (model 3). Finally, the significance of the association could not be altered when gestational age, pregnancy in vitro, parity before, and educational level were entered into the model (model 4).
Linear Regression Statistics Showing Estimated Change in Mean Performance of Physical Fitness Components per Month Increase of Exclusive Breastfeeding, for Boys and Girls
Model 1: children's BMI (8 years) + low birth weight; model 2: model 1 + prepregnancy BMI status + GWG; model 3: model 2 + gestational age + pregnancy in vitro + parity before + educational level.
Unadjusted.
Hierarchical binary logistic regression analysis was conducted to investigate the effect of exclusive breastfeeding (<1 versus ≥6 months) on performances (average/high versus low) in all PF tests and as a total index of PF, by sex. The initial analysis (model 1, Table 4) revealed that (with the exception of speed test in girls) children who were exclusively breastfed had 10%–40% increased odds for average/high performances in PF tests in comparison with those who were breastfed <1 month. When the existence of low birth weight and children's BMI were added in the analysis (Table 4, model 2), the previous findings could not be altered significantly. After additional adjustment for pregnancy BMI status and GWG (model 3), the results remained almost the same. Finally, when gestational age, pregnancy in vitro, parity before, and educational level were included in the analysis (model 4), the influence of exclusive breastfeeding on PF test performances was slightly decreased, but remained statistically significant.
Results (Odds Ratio, 95% Confidence Interval) from Logistic Regression Models to Evaluate the Association of Exclusive Breastfeeding (<1 Versus ≥6 Months) with Low Performance in Physical Fitness Components
Model 1: unadjusted; model 2: adjusted for children's BMI + low birth weight; model 3: model 2 + prepregnancy BMI status + GWG; model 4: model 3 + gestational age + pregnancy in vitro + parity before + educational level.
CI, confidence interval; PF, physical fitness; OR, odds ratio.
Discussion
To the best of our knowledge the current study is among few studies that aimed to investigate the association of exclusive breastfeeding with a wide range of PF test performances in children. Because early infant feeding practices are possibly modifiable by parental decision, it is crucial to investigate the potential effect of breastfeeding on PF in order to support public health interventions. Data from this representative cohort revealed that (1) exclusive breastfeeding was favorably associated with all PF components, in both sexes, and (2) exclusive breastfeeding ≥6 months increased the odds of average/high performances (it can be considered a fitness zone) in overall PF and at separate PF components in childhood, even after adjusting for several potential confounders. Specifically, when examining separate PF components, we found a positive association between exclusive breastfeeding and CRF, lower body explosive strength, upper body explosive strength, and speed. Moreover, it seems that a longer duration of exclusive breastfeeding might have an increasing benefit in all PF components.
In the current study, we included several potential risk factors that influence exclusive breastfeeding such as prepregnancy BMI status, GWG, gestational age, pregnancy in vitro, parity before, and educational level. Moreover, we performed additional analyses (four models) to examine whether these factors could affect the association between breastfeeding and PF performances.
As far as we know, four studies have examined the influence of mixed or exclusive breastfeeding on PF components among children. Most of these studies have investigated the association between breastfeeding and CRF,21–23 while one study has examined the association between breastfeeding and muscular strength. 24 Our study revealed that exclusive breastfeeding is favorably associated with CRF, in both sexes. In line with our findings, two studies concluded that a longer period of breastfeeding showed a positive effect on CRF in children.21,22 Specifically, a study by Labayen et al., involving 1,996 participants aged 9–15 years, speculated that exclusive breastfeeding ≥3 months had a beneficial effect on CRF, 21 while another study by Vafa et al. revealed a favorable association between exclusive breastfeeding ≥6 months and CRF in children aged 7–8 years. 22 On the contrary, a research by Lawlor et al., which examined the influence of mixed breastfeeding on CRF in 3,612 children aged 9 years, did not find a significant association. 23 Also, although a study assessing CRF with the use of 20mSRT in 2,567 adolescents aged 12.5–17.5 years showed a significant association between the duration of mixed breastfeeding and CRF, this association could not be confirmed once exclusive breastfeeding was considered. 24 The reasons for the differing results among the studies could be attributed to the discrepancy among the methods of measuring CRF, the different age ranges, and whether exclusive or non-exclusive breastfeeding was considered. Based on scientific evidence, human milk contains components such as polyunsaturated fatty acids, which are not present in formula milk; adipokines and prostaglandin J2 could explain, at least in part, the favorable effect of breastfeeding on CRF. 20
Our findings proposed a favorable effect of exclusive breastfeeding on muscular strength (lower and upper body explosive strength). Given that muscular strength is clearly influenced by morphological factors such as body mass, for the current study we used BMI and low birth weight as confounders to adjust for body composition differences. 29 There is only one study that examined the association of breastfeeding with muscular strength. Specifically, our results are in line with Artero et al., which suggested that longer breastfeeding is significantly associated with better performance in the SLJ test in adolescents after adjusting for numerous potential confounders. 24 Moreover, the results of the previous study did not show a positive association between the upper body explosive strength (as measured via handgrip strength test) and exclusive breastfeeding. The different tests that have been used to measure upper body strength could justify the different results between the current study and that of Artero et al. 24 It is well known that, in large part, fiber type transformations and muscle growth take place postnatally, and also the number of muscle fibers is fixed, at least to some extent, during the perinatal period. 30 Furthermore, it is considered that although locomotion occurs at the age of ∼1 year, a stepping pattern may be present already at birth or shortly after. 31 As a consequence, we suppose that the feeding pattern throughout the first months of life could influence the development of the muscle system.
Our results showed a small but advantageous influence of exclusive breastfeeding on speed test. Furthermore, it proposed that children who were exclusively breastfed had almost 30% increased odds of average/high performances in comparison with those who were breastfed <1 month, but only in boys. The performance in speed test is predisposed by anthropometric indices such as BMI (e.g., overweight, obesity), muscle growth, motor skills, and other factors. 28 Exclusive breastfeeding is possibly a crucial factor in reducing the risk of obesity during childhood. 19 Children use their large muscle groups when utilizing their motor skills, such as running. A study involving infants speculated a favorable association between duration of exclusive breastfeeding and the motor abilities of children. 32 The significance of diet quality for gross motor development in infancy points out that feeding patterns during the early stages of life could influence the development of motor skills. 33 Human milk components that promote offspring's health, such as enzymes, hormonally active proteins (e.g., insulin-like growth factor-1 [IGF-1]), essential fatty acids, etc., are missing in formula milk.8–10 In sum, the advantageous effects of exclusive breastfeeding on children's growth and feeding patterns could partly explain the current findings.
The main strengths of this work are: (1) it explored the potential association between exclusive breastfeeding and several PF components, taking into account a large, representative sample equally distributed (about 500 dyads per year) throughout the study period (1997–2007); (2) a well-balanced sex distribution, which makes sex-specific analyses feasible; (3) an adjustment for several factors that possibly confound the association of exclusive breastfeeding with PF.
Limitations
The information that was collected during telephone interviews was self-reported. Therefore, this might represent a limitation of the study. Specifically, this could be attributed to deliberate over-reporting, underreporting, or recall bias in self-reported prepregnancy anthropometric data (body weight and height). Also, retrospective maternal recall of breastfeeding duration could be subject of some recall bias. Nevertheless, the validity of maternal recall of duration of breastfeeding has been shown to be very high, several years later. 34 Moreover, there might be a degree of selection bias in the analysis as the mothers who had exclusively breastfed might have encouraged a different pattern and degree of physical activity with their children, and as a consequence, the difference in outcomes with regard to the duration of exclusivity might not be entirely valid.
Conclusions
Among 8- to 9-year-old Greek children, we found a small but favorable and significant association of exclusive breastfeeding with all PF components (lower and upper body strength, CRF, and speed), in both sexes, after adjusting for several potential confounders. In view of the fact that exclusive breastfeeding is a modifiable factor, health care professionals should recommend mothers to exclusively breastfeed as long as possible. Our findings support the recommendation that infants should be exclusively breastfed for 6 months and longer.
Footnotes
Acknowledgments
The authors wish to thank the study subjects for their willingness to participate. We are also very grateful to Mrs. Stavroula Parastatidou, Markella Symeopoulou, and Mema Lampropoulou for their assistance with data collection.
Disclosure Statement
No competing financial interests exist.
