Published online September 1, 2008
PEDIATRICS Vol. 122 No. 3 September 2008, pp. e728-e736 (doi:10.1542/peds.2007-2573)
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ARTICLE

Objectively Measured Physical Activity and Bone Strength in 9-Year-Old Boys and Girls

Luís B. Sardinha, PhDa, Fátima Baptista, PhDa and Ulf Ekelund, PhDb,c

a Exercise and Health Laboratory, Faculty of Human Movement, Technical University of Lisbon, Lisbon, Portugal
b Medical Research Council Epidemiology Unit, Institute of Public Health, University of Cambridge, Cambridge, United Kingdom
c School of Health and Medical Science, Örebro University, Örebro, Sweden


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. The purpose of this work was to analyze the relationship between intensity and duration of physical activity and composite indices of femoral neck strength and bone-mineral content of the femoral neck, lumbar spine, and total body.

METHODS. Physical activity was assessed by accelerometry in 143 girls and 150 boys (mean age: 9.7 years). Measurement of bone-mineral content, femoral neck bone-mineral density, femoral neck width, hip axis length, and total body fat-free mass was performed with dual-energy radiograph absorptiometry. Compressive [(bone-mineral density x femoral neck width/weight)] and bending strength [(bone-mineral density x femoral neck width2)/(hip axis length x weight)] express the forces that the femoral neck has to withstand in weight bearing, whereas impact strength [(bone-mineral density x femoral neck width x hip axis length)/(height x weight)] expresses the energy that the femoral neck has to absorb in an impact from standing height.

RESULTS. Analysis of covariance (fat-free mass and age adjusted) showed differences between boys and girls of ~9% for compressive, 10% for bending, and 9% for impact strength. Stepwise regression analysis using time spent at sedentary, light, moderate, and vigorous physical activity as predictors revealed that vigorous physical activity explained 5% to 9% of femoral neck strength variable variance in both genders, except for bending strength in boys, and ~1% to 3% of total body and femoral neck bone-mineral content variance. Vigorous physical activity was then used to categorize boys and girls into quartiles. Pairwise comparison indicated that boys in the third and fourth quartiles (accumulation of >26 minutes/day) demonstrated higher compressive (11%–12%), bending (10%), and impact (14%) strength than boys in the first quartile. In girls, comparison revealed a difference between the fourth (accumulation of >25 minutes/day) and first quartiles for bending strength (11%). We did not observe any relationship between physical activity and lumbar spine strength.

CONCLUSIONS. Femoral neck strength is higher in boys than girls. Vigorous intensity emerged as the main physical activity predictor of femoral neck strength but did not explain gender differences. Daily vigorous physical activity for at least ~25 minutes seems to improve femoral neck bone health in children.

Key Words: bone strength • children • physical activity

Abbreviations: BMC—bone-mineral content • BMD—bone-mineral density • DEXA—dual-energy radiograph absorptiometry • HAL—hip axis length • FNW—femoral neck minimal width

Fractures caused by the metabolic disease osteoporosis are a major public health problem.1 Skeletal growth in size, shape, and architecture and subsequent bone loss and architectural disruption are important determinants of later osteoporosis, and there is evidence to suggest that osteoporosis and the risk of fractures may be reduced by maximizing the accrual of peak bone strength during childhood and adolescence.2, 3 The critical years for skeletal growth and acquisition of peak bone strength seem to lie in the 2 first decades of life with the acquisition of peak bone mass.4, 5 Although bone mass, expressed by bone-mineral content (BMC) and bone-mineral density (BMD), in children is largely determined by genotype,6 there is persuasive evidence that modifiable lifestyle factors, such as physical activity, particularly weight-bearing physical activity, can have a significant impact on bone mass acquisition and structural (geometric) adaptation in children, adolescents, and young adults.7–12 However, habitual physical activity as a behavior is multidimensional and complex, making it difficult to assess, and most previous studies examining the relationship between physical activity and bone in the young population have assessed physical activity by self-report methods and bone with density-based measurements.7–15 Self-report assessment of physical activity is imprecise, particularly in young children. Consequently, it is normally recommended that, in children of 10 to 11 years of age or younger, self-report methods should be avoided because the cognitive capacity of children is usually insufficient to allow accurate and reliable self-assessment of their behavior.16, 17 Moreover, bone measurements only by means of BMC or BMD do not provide information about structural dimensions, a factor that is determinant to bone strength.18

Objective assessments of physical activity using activity monitors based on accelerometry provide valid information on the frequency, intensity, and duration of physical activity19; have been shown to be valid for the assessment of the total amount of physical activity in free-living children20; and are feasible to use in large-scale epidemiologic studies.21 Furthermore, because these instruments accurately measure the ground reaction forces during various speeds of walking, running, and other activities that are weight bearing in children, they may be particularly beneficial when assessing habitual physical activity and its subcomponents in relationship to material and structural properties of bone in children.22 Therefore, the purpose of the present study was to examine the cross-sectional associations between different components of objectively assessed physical activity in relation to dual-energy radiograph absorptiometry (DEXA) estimates of composite strength indices of femoral neck and measures of total body, lumbar spine, and femoral neck BMC using a randomly selected population-based cohort of 297 healthy, 9- to 10-year-old Portuguese children.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Participants
The subjects participating in this study were all participants in the European Youth Heart Study, a multicenter, mixed longitudinal study aimed to examine environmental and lifestyle influences on cardiovascular and metabolic disease risk factors in children and adolescents. The design, selection procedures, and methods have been described previously.21, 23 Briefly, a defined population of children was identified, and from this population a 2-stage cluster sample of children was randomly selected. The primary sampling unit was schools, and the secondary unit was school registers. At least 20 schools were randomly selected from local authority lists within appropriate age, gender, and socioeconomic strata using a probability proportional to school size. A total of 530 healthy children from the county of Madeira, Portugal, were sampled and invited to participate in the study along with their parents. Of these, 72 children refuse to wear the activity monitor, 96 children were excluded because of not meeting the inclusion criteria for physical activity measurements (see below), and 37 children were excluded because of faulty activity monitors. Complete anthropometric, DEXA body composition measurements, as well as clinical and physical activity measurements, were available in 293 children (150 boys and 143 girls). There were no significant differences (P > .05) in body weight, height, BMI, sum of skinfolds, and waist circumference between those with complete data compared with the rest of the children. The Faculty of Human Movement's Human Subjects Institutional Review Board approved the study, and parents or legal guardians provided written informed consent.

Physical Activity
Physical activity was assessed with a uniaxial accelerometer (model WAM 6471, formerly known as the CSA activity monitor [Manufacturing Technology Incorporated, Fort Walton Beach, FL]). The accelerometer is a small (5.1 x 3.8 x 1.5 cm), light-weight (~45 g) instrument, that has been validated previously in children and adolescents under free-living conditions against physical activity-related energy expenditure obtained by the doubly labeled water method.20, 24 The accelerometer measures vertical accelerations from 0.05 to 2.10 G and is equipped with a pass-band filter, which discriminates human movements from vibrations. Activity data from the accelerometer were sampled on a minute-by-minute basis. The accelerometer was secured on the right hip, using an elastic belt. The subjects were asked to wear the accelerometer during the daytime for 2 weekdays and 2 weekend days, except during water activities.

Activity data were analyzed and processed by using a special written program (MAHUffe, www.mrc-epid.cam.ac.uk). The output from the program included accumulated time spent at physical activity of moderate- and high-intensity levels. In addition, the total amount of time (minutes) registered each day was recorded. The total amount of physical activity was expressed as total counts divided by registered time, that is, counts/minute (counts · minute–1 · day–1). All of the activity data were averaged over the 4-day period. Subjects were excluded if they failed to provide a minimum of 3 days of ≥600 minutes of accelerometer data. The primary physical activity outcome variable was counts · minute–1 · day–1. Secondary outcome variables were time (minutes·day–1) spent sedentary and time spent at light, moderate, and vigorous intensity of physical activity. Intensity thresholds for light, moderate, and vigorous intensity were the same as those used previously in the European Youth Heart Study.25 An arbitrary cutoff value, used previously in adolescents,23 of ≤100 counts·minute–1 was used as an indicator of sedentary behavior.

Body Size
Standing height (to the nearest centimeter) was measured on a stadiometer (Secca 770, Hamburg, Germany) without shoes. Body weight (kilograms), total fat (kilograms), and total fat-free mass (kilograms) were determined from a total body scan by DEXA (Hologic, Waltham, MA; pencil beam, software 5.73) in the fasted state with children dressed in their underwear. BMI was calculated as body weight in kilograms divided by height in meters squared.

Sexual maturation was assessed by the investigators using Tanner's 5-stage scale for breast development in girls and pubic hair in boys. Children were stratified as prepubertal (Tanner stage 1) or having started puberty (Tanner stage 2).

Mineral and Structural Bone Measures
Total body, lumbar spine (L2 to L4), and left hip (femoral neck) bone-mineral evaluations were made using a DEXA (QDR-1500, high-speed performance mode, software 5.73 for total body and 4.76 for lumbar spine and femoral neck). None of the children reported a history of bone fracture. Assessment of femoral neck minimal width (FNW) and hip axis length (HAL) was obtained from the DEXA hip scan. FNW was determined manually in its narrowest section perpendicular to the hip axis using the tools of the software. Composite measures of femoral neck strength, namely, compressive, bending, and impact strength, were estimated as suggested by Karlamangla et al26 and have been described previously.27 These measures reflect the ability of the femoral neck to withstand axial compressive and bending forces and the ability to absorb energy from an impact.

Formula

Formula

Formula
Quality assurance tests were performed each morning. The coefficients of variation of the spine phantom BMD was 0.3%. Precision errors were estimated from 2 measurements by repositioning 30 subjects. The coefficient of variation of BMD was 1.7% for femoral neck BMD.

Statistical Analysis
Data were analyzed by using SPSS 12.0 for Windows statistical software (SPSS Inc, Chicago, IL). Differences between boys and girls were examined by independent-samples t test. Relationships between physical activity variables and bone measures were studied by bivariate, multivariate, and categorical analysis stratified by gender. The relationship between fat-free mass and physical activity were conducted by partial correlation adjusted for age and body weight. The independent association between fat-free mass with BMC variance was examined by linear regression analysis after adjustment for bone area, height, weight, and age. Similarly, the independent associations between fat-free mass and femoral neck structural measures were analyzed by linear regression after adjustment for body weight and age. Partial correlation was used to measure the linear association between physical activity variables, (ie, time spent at sedentary, light, moderate, and vigorous physical activity) and bone variables, (ie, total body, lumbar spine, and femoral neck BMC, as well as femoral neck structural measures). For this purpose, analyses between physical activity and BMC measures were adjusted for bone area, body height, and body weight to avoid the possibility of size-related artifacts in the analysis of bone-mineral data.28 Adjustments were further made for age and total fat-free mass. In preliminary analyses, additional adjustments were made for sexual maturity (2 categories). However, this adjustment did not change the magnitude or direction of the observed associations and were excluded from the final models. Stepwise multiple regression analyses were used to determine the independent contribution of physical activity variables on the variance of all of the BMC and femoral neck structural variables after adjustments for bone area, height, weight, fat-free mass, and age and with femoral neck structural measures after adjustments for age and fat-free mass. Physical activity variables, which significantly contributed to the explained variance in bone variables, were then used to categorize boys and girls into quartiles to compare differences between high and low active groups in bone measures. Pairwise comparisons were made by means of simple contrasts with the first quartile as the reference category. The level of statistical significance was set at a P value of <.05.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Descriptive
Descriptive characteristics of the children are displayed in Table 1. No significant differences were observed between boys and girls according to age, weight, and height; however, fat-free mass was significantly higher (P < .001) and fat mass significantly lower (P = .001) in boys. Total BMC (P = .039) and femoral neck measures, namely, BMC (P < .001), bone area (P = .039), BMD (P < .001), and structural strength (P < .001), were significantly higher in boys than in girls.


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  		TABLE 1 Subject Characteristics

 
A description of children's physical activity is presented in Table 2. The accelerometry-determined measures of physical activity showed that boys spent significantly more time in moderate and vigorous intensity of physical activity than girls (P < .001), whereas girls spent mort time in light intensity physical activity and sedentary activity (P < .001). The total amount of physical activity (counts · minute–1 · day–1) was also significantly higher in boys (P < .001).


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  		TABLE 2 Time Spent in Physical Activity

 
Bivariate Correlation Analysis
Partial correlation coefficients between physical activity and bone measures are presented in Table 3. No significant associations were observed between lumbar spine BMC and any of the physical activity variables. Femoral neck BMC and total body BMC were significantly associated with time spent at vigorous intensity physical activity in both genders (r = 0.17 to 0.23; P < .05).


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  		TABLE 3 Partial Correlations Among Fat-Free Mass, Bone, and Physical Activity Measures

 
Correlation coefficients for the relationships between femoral neck structural measures and physical activity variables were slightly higher in boys than in girls. In boys, significant and inverse associations between femoral neck structural measures and time spent at sedentary activity (r = –0.17 to –0.21; P < .05) and significant and positive associations for time spent at moderate (r = 0.21 to 0.23; P < .05) and vigorous physical activity (r = 0.19 to 0.34; P < .05) were observed. In girls, the 3 femoral neck structural measures were only significantly associated with time spent at vigorous intensity physical activity (r = 0.22 to 0.26; P < .05). Vigorous intensity of physical activity was the only physical activity variable significantly associated with fat-free mass, and this association was only observed in girls.

Linear Regression Analysis
A summary of the results from the multiple linear regression analyses are presented in Tables 4 and 5. Fat-free mass explained a higher proportion of bone variability in femoral neck variables than in the lumbar spine and in the whole body (ie, total BMC). This was more pronounced in girls (7.7%–19.2% vs 1.0%–2.9%) than in boys (1.1%–4.4% vs 1.1%–1.9%; Table 4).


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  		TABLE 4 Prediction of Bone Variance According to Fat-Free Mass in Boys and Girls

 

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  		TABLE 5 Physical Activity Predictors of Bone Variance in Boys and Girls

 
Physical activity explained a small but significant amount of the variance in total BMC, femoral neck BMC, and femoral neck strength measures. Time spent at vigorous intensity physical activity explained 0.5% to 0.6% of the variance of total body BMC, whereas the magnitude of the explained variance was between 1.3% and 9.3% for femoral neck variables, except for femoral bending strength in boys. In this structural measure, time spent at moderate intensity physical activity explained 3.2% (whereas time spent at vigorous intensity physical activity explained 0.7% of the variance in boys). In general, the coefficient of determination was higher for femoral neck BMC than for total body BMC and in boys compared with girls (Table 5).

Categorical Analysis
Differences in total body and femoral neck bone measures categorized by quartiles of vigorous intensity physical activity are presented in Table 6. Pairwise comparison indicated a 5% to 6% greater BMC of the femoral neck in boys and girls in the most active quartile of vigorous intensity physical activity when compared with boys and girls in the lowest quartiles, respectively. No significant differences were observed between groups for total BMC. Boys in the third and forth quartiles of vigorous intensity physical activity demonstrated significantly higher values of compressive (11%–12%), and impact strength (14%) than boys in the first quartile when comparing these femoral neck structural measures. Significant differences (10%–11%) were also observed between the lowest and the highest quartiles of vigorous intensity physical activity in both genders, considering bending strength of the femoral neck.


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  		TABLE 6 Total Body BMC, Femoral Neck BMC, and Structural Measures According to Quartiles of Vigorous Physical Activity and Percentage Change From the Least Active Quartile

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Several previous studies in children and adolescents have reported positive associations between physical activity and bone density and architecture in boys and in girls.11, 29–38 However, most of these studies have relied on self-reported measures of physical activity, which may be insufficient to support the current physical activity guidelines for children and adolescents.39, 40 Our results suggest that the intensity of physical activity needs to be vigorous to influence bone strength of the femoral neck and that children may need to accumulate ~25 minutes of vigorous intensity per day to improve their bone strength by changing bone mass and/or geometry.

We found that total body and femoral neck BMC are higher in boys than in girls (5% and 12%, respectively). However, when BMC is adjusted for bone area, body weight, and height, the differences between boys and girls are attenuated to ~3% in the whole body. Lumbar spine BMC is 4% higher in girls than in boys after these adjustments. When BMC measures are additionally adjusted for total fat-free mass, girls demonstrate proportionally higher BMC in the total body (2%) and lumbar spine (6%), whereas the difference between boys and girls in femoral neck BMC decreased from 12% to 6%. Composite indices of the femoral neck, which integrate bone size and body size with bone density, revealed that boys have higher bone strength indices at this skeletal site than girls, also after adjustment for fat-free mass. These results indicate that total body BMC and, to some extent, also femoral neck BMC, are higher in boys than in girls, as a consequence of their higher fat-free mass and that the differences in the lumbar spine are less dependent on fat-free mass in this group of 9- to 10-year-old children.

Fat-free mass contributed to a greater extent to the whole body and especially to femoral neck bone variance in girls compared with boys despite their lower total fat-free mass. This observation was not affected by adjustment for vigorous physical activity. In contrast, vigorous physical activity explained a higher proportion of femoral neck variables in boys compared with girls.

Although the bone adaptive responses are affected by the amplitude, frequency, distribution, and duration of the bone's loading history, it is commonly believed that maximum strains during vigorous activities have the greatest influence on bone.41 Types of activities usually performed by children equal to our definition of vigorous intensity (ie, >4000 counts/minute) and accurately measured by accelerometry are brisk walking (>6 km/hour) and all activities including vertical movement of the body, such as jogging, running, and jumping (eg, hopscotch). Despite higher levels of vigorous activities in boys than in girls (29 vs 18 minutes/day), this did not explain the between-gender differences observed. After adjustment for time spent in vigorous physical activity, total body BMC and lumbar spine BMC remained significantly higher in girls, whereas femoral neck BMC and femoral neck strength indices were higher in boys.

Two recent studies demonstrated the importance of physical activity or sports activities in determining femoral neck peak bone status in adolescents29 and young adult boys.10 Failure to observe this association in girls and women may reflect their lower participation in such activities. A novel finding in the present study is that boys with a cumulative participation in vigorous intensity physical activity <12 minutes/day (lowest quartile) revealed similar or even greater femoral neck bone strength measures than the most active quartile of girls (ie, >25 minutes/day of vigorous intensity physical activity). After adjusting for body size and physical activity, it seems that femoral neck strength is greater in boys than in girls, which would imply greater bone strength, as suggested previously in adults.42

Vigorous intensity physical activity accounted for ~1% of the variance in total body BMC and for 4% to 9% of the variance in femoral neck measures in both genders, with exception for femoral neck impact strength in boys. These results indicate that physical activity is an important predictor of femoral neck measures when performed at vigorous intensity levels. Engagement in physical activity at this intensity provides a compensation for the negative effect that time spent at sedentary activity has on femoral neck strength indices in boys. The bivariate association observed in boys between time spent at sedentary activity and femoral neck strength was not significant in the multiple regression models, whereas time spent at vigorous intensity of physical activity remained statically significant.

These findings are consistent with previous observations in 4- to 6-year-old children11, 12 and 11-year-old children.38 Similar to our observations, vigorous intensity of physical activity was the variable most strongly associated with bone measures, and the explained variances (1.5%–9% for hip and spine BMC and BMD; ~4% for proximal femur cross-sectional area and section modulus-Z) were similar to ours. Similar to our observations, results were more consistent for femoral neck bone mass than for lumbar spine. However, in the study of Janz et al,11 vigorous intensity of physical activity explained more of the variability in BMD and BMC in girls than in boys. This difference between studies may be explained by a more advanced maturation in girls than in boys in the present study, suggesting a greater influence of hormones on bone mass variability in girls than in boys. The greater adjusted BMC in the lumbar spine in girls compared with boys might be an expression of this type of influence. Boys usually present more lumbar spine BMD than girls of the same biological age,30 and skeletal mineralization accelerates at the onset of puberty in the spine and less in the femoral neck.43, 44 However, our relatively crude measure of biological maturation did not influence the observed associations.

Others have concluded that moderate intensity of physical activity exerts the greatest influence on bone size and density.38 However, although using the same objective measurement technique, this study defined moderate and vigorous intensity activity differently. Indeed, their definition of moderate intensity is similar to our threshold for vigorous intensity activity, which may then suggest that the findings are comparable.

Our categorical analysis according to time spent in vigorous intensity of physical activity allowed examination of the minimum of accumulated time at this intensity level associated with significant positive results in bone measures. This analysis suggested that children who accumulated ~25 minutes/day had higher values (10%–14%) of femoral neck strength indices than children of the lowest quartile of vigorous intensity physical activity. However, in girls these differences were only significant for bending strength (11%). These results suggest a threshold below which the relationship between bone measures and physical activity might be weak. Despite the suggestion that a 10-minute increase in daily vigorous activity in young children would result in hip BMC increases of 3%, data have suggested that a bone mass gain will be observed only in young girls and boys who spent ≥32 or 40 minutes of vigorous activity per day, respectively.11 In our study using a slightly different size-adjusted BMC method, the results were similar. Boys who accumulated ≥42 minutes/day (fourth quartile) demonstrated significantly higher values of femoral neck BMC (6%) than boys who accumulated ≤12 minutes/day (first quartile). Similarly, girls who accumulated ≥25 minutes/day (fourth quartile) revealed significantly higher values of femoral neck BMC (5%) than girls who accumulated of ≤8 minutes/day (first quartile).

Strong associations between vigorous physical activity and femoral neck measures may be attributable, in part, to the objective evaluation of physical activity by means of hip displacement but also by the fact that this skeletal site seems to be considerably affected by mechanical factors during the peak bone mass accrual. Lumbar spine, with more trabecular bone, is more influenced by metabolic and hormonal factors.45–47 An example of this hormonal influence is the chronic condition of hypoestrogenism, with spine being the skeletal region with more deleterious effects.48–50 Some studies in children and adolescents have indicated an association between weight-bearing physical activity and BMC of the spine9, 11 regardless of hormonal dysfunction.51, 52 However, in general, the femoral neck revealed a greater response to increased weight-bearing physical activity than the spine.29

As in all observational studies, our data are only suggestive of a causal association between physical activity and bone health. However, it is unlikely that these associations are attributable to chance. The ability to detect the association between physical activity and bone health that we report in the present study depends on several factors. These include the precision of exposure and outcome measurement, the sample size, and the magnitude of the association between exposure and outcome. The present study was undertaken in a large, randomly selected population-based cohort of children for whom objective assessments of physical activity were available. Physical activity was assessed through accelerometry. This method has been validated previously in children against the doubly labeled water method,20 which is considered by many as the gold-standard method for assessing free-living physical activity and related energy expenditure. Moreover, accelerometry is considerably more reliable and valid than subjective techniques, such as questionnaire and interview in children.17 One limitation of our study may include biological maturational differences between boys and girls of the same chronological age that were not accounted for by our relatively crude measure of maturation (ie, Tanner stage). We cannot, therefore, rule out the possibility that some residual confounding by maturation exist.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Femoral neck measures were higher in boys than in girls. Vigorous intensity emerged as the main physical activity predictor of femoral neck measures but did not explain gender differences in this skeletal site. Beyond an independent effect of fat-free mass in the skeleton of girls, daily vigorous intensity physical activity for ≥25 minutes seems to be related to improved femoral neck bone health in children.


   FOOTNOTES
 
Accepted Apr 17, 2008.

Address correspondence to Luís B. Sardinha, PhD, Exercise and Health Laboratory, Faculty of Human Movement, Technical University of Lisbon Estrada da Costa, 1495-688 Cruz Quebrada, Portugal. E-mail: lsardinha{at}fmh.utl.pt

The authors have indicated they have no financial relationships relevant to this article to disclose.


What's Known on This Subject

The current physical activity recommendations for children are based essentially on cardiovascular health promotion. This study presents some support regarding how much weight-bearing physical activity is needed to obtain bone-health benefits in children.

 

What This Study Adds

Vigorous intensity emerged as the main physical activity predictor of femoral neck bone health in children. Boys and girls may need to accumulate 25 minutes of vigorous intensity per day to improve their bone strength by changing bone mass/or geometry.

 


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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