This study was performed at the Department of Nutrition, Federal University of Pernambuco, 50670-901 Recife, PE, Brazil
Permanent deficits in handgrip strength and running speed performance in low birth weight children†
Article first published online: 7 NOV 2012
Copyright © 2012 Wiley Periodicals, Inc.
American Journal of Human Biology
Volume 25, Issue 1, pages 58–62, January/February 2013
How to Cite
Moura-Dos-Santos, M., Wellington-Barros, J., Brito-Almeida, M., Manhães-de-Castro, R., Maia, J. and Góis Leandro, C. (2013), Permanent deficits in handgrip strength and running speed performance in low birth weight children. Am. J. Hum. Biol., 25: 58–62. doi: 10.1002/ajhb.22341
- Issue published online: 18 DEC 2012
- Article first published online: 7 NOV 2012
- Manuscript Accepted: 10 OCT 2012
- Manuscript Revised: 4 OCT 2012
- Manuscript Received: 9 AUG 2012
- National Council for Scientific and Technological Development (CNPq). Grant Number: 501619/2009-7
- the Coordination for the Improvement of Higher Level -or Education- Personnel (CAPES). Grant Number: 2317/2008
- the State of Pernambuco Science and Technology Support Foundation (FACEPE). Grant Number: APQ-0575-4.05/08
The main goal of this study was to verify the influence of low birth weight (LBW) on the physical fitness of children aged 7–10 years. The comparisons were subsequently adjusted for chronological age, gender, physical activity (PA), and body composition.
A total of 356 children of both genders born in Vitoria de Santo Antão (Northeast of Brazil) were divided into two groups according to their birth weight (LBW < 2.500 g, n = 100, and normal birth weight, NBW ≥ 3.000 g and ≤ 3.999 g, n = 256). Body composition measurements included body weight, height, body mass index, triceps, and subscapular skinfolds, and body fat percentage (%BF). PA was assessed by a questionnaire. Physical fitness was assessed by handgrip strength, muscle endurance, explosive power, flexibility, agility, maximal oxygen consumption (VO2max), and running speed.
LBW children were shorter, lighter, had lower fat-free mass, muscle strength, and running speed but a higher VO2max than the NBW group. The differences in body weight (P = 0.507), height (P = 0.177), fat-free mass (P = 0.374), and VO2max (P = 0.312) disappeared when adjusted for covariates. The differences in right and left handgrip strength (P < 0.01) and running speed (P < 0.01) remained significant even when controlled for age, gender, height, fat-free mass, and PA.
This combined analysis suggests that LBW alone can be not considered as a biological determinant of growth, body composition, or physical fitness in children, but is a predictor of muscle strength and running speed. Am. J. Hum. Biol., 2013. © 2012 Wiley Periodicals, Inc.
Over the last years, epidemiological, clinical and experimental studies have focused on the association between early life events and the normal trajectory of growth, body composition, physical activity (PA) levels, physical fitness and the risk of adult disease (Barker et al., 2005; Chomtho et al., 2008; Ortega et al., 2009; Ridgway et al., 2011). Previous studies have shown that birth weight is an important marker of the environmental status of mothers during gestation (Gluckman et al., 2007, 2009). Low birth weight (LBW, birth weight < 2500 g) can result from a short gestation or environmental stimuli or insults (for example, undernutrition, hormones, antigens, drugs, or alcohol). Inverse relationships between birth weight and the risk of metabolic diseases (glucose intolerance, obesity, and dyslipidemia) and heart disease in adulthood have been reported (Barker, 1999; Barker et al., 2005). However, like LBW, rapid body weight gain during childhood is also related with various indicators of metabolic syndrome (Singhal et al., 2003) and may be further exacerbated by a hypercaloric diet and low levels of PA and physical fitness (Wells, 2010).
Physical fitness is a measure of the body's abilities related to both health (leisure activities) and sports performance. Physical fitness is often related to components such as cardiorespiratory fitness, muscle strength, muscle endurance, body composition, agility, and flexibility (Beunen et al., 1997). Low levels of physical fitness may induce a more sedentary lifestyle and an increased risk of metabolic disease (Beunen et al., 1997). However, high maximal oxygen consumption (VO2max), as an indicator of cardiorespiratory fitness, has been associated with a low predisposition to cardiovascular and metabolic diseases (Carnethon et al., 2009). Muscle strength and endurance are related to large muscle mass, reduced fat mass and a high resting metabolic rate (Vuori, 2001). In addition, flexibility has been related to reduced injury risk and the prevention or reduction of postexercise soreness (Hopper et al., 2005). Physical fitness is directly associated with regular PA and more benefits have been observed for higher active lifestyles (Mota et al., 2002). Recently, it has been shown that physical fitness can also be influenced by birth weight (Keller et al., 2000; Kriemler et al., 2005; Rogers et al., 2005).
Lower birth weight has been related with reduced physical performance in tests to evaluate physical fitness, including muscle strength, muscle endurance and cardiorespiratory fitness in children and adolescents (Ridgway et al., 2011). Birth weight was positively associated with both lean body mass and total body fat at 9–10 years of age in both sexes (Rogers et al., 2006). Extremely low birth weight (ELBW < 999 g) infants show a lower running economy, aerobic capacity, and flexibility compared with their normal birth weight (NBW) peers (Baraldi et al., 1991). Similarly, birth weight and aerobic fitness (measured in laps completed until voluntary exhaustion by a 20-m shuttle run test) were positively related in young males and females (aged 12 and 15 years; Boreham et al., 2001). Aerobic capacity, strength, flexibility and activity level were lower in ELBW adolescents (17-years-old) than their NBW peers (Rogers et al., 2005). Female ELBW adolescents (aged 13–18.5 years) demonstrated low performances in handgrip strength tests (as an indicator of muscle strength) after adjusting for body fat percentage (%BF; Ortega et al., 2009). Indeed, birth weight may induce reduced physical fitness, including low muscle mass-induced muscle strength deficits and low aerobic capacity-induced insufficient cardiorespiratory fitness (Andersen et al., 2009). However, the associations between birth weight and physical fitness is mostly limited to extreme groups (extremely LBW) and little is known about the influence of a less deleterious birth weight (LBW) range on physical fitness in children.
In this study, the influences of LBW on the body composition and physical fitness of children aged 7–10 years were evaluated. The comparisons were subsequently adjusted for chronological age, sex, PA, and body composition. Our hypothesis is that birth weight is a significant predictor of growth (height and weight), body composition (% fat mass and lean body mass), and physical fitness measures during childhood and that an environmental factor (PA levels) and biological variables (age, sex, and size variables) may condition these relationships.
Material and Methods
This study was conducted in the city of Vitória de Santo Antão, which is located in a traditional and economically poor rural zone in the state of Pernambuco, in northeast Brazil. The sample size was estimated in Epi Info 6.04 given the following conditions: an error of ±5%, a power of 80%, and a relative risk of 2.0 for events in low-birth weight versus NBW subjects, that is, a ratio of 1:2. A total of 356 children (196 boys and 160 girls) aged 7–10 years old were evaluated. The sample was divided into two groups according to their birth weight: LBW from 1.500 to 2.500 g (n = 100) and NBW from 3.000 to 3.999 g (n = 256). All measurements were carried out during a 6-month period from March to November 2009, according to the school calendar. No seasonality is to be expected in the PA measures and physical fitness given that the temperature and weather conditions are stable during this period.
The birth weights were obtained from health booklets in which this information was recorded by nurses and/or pediatricians. Written informed consent was obtained from the parents or legal guardians of each child. This study was approved by the ethics committee of thelocal health authority (Center of Health Science, Federal University of Pernambuco, protocol number 0175.0.172.000-09).
Anthropometry and body composition
The body weight of the lightly dressed and barefooted subjects were measured to the nearest 0.1 kg with a digital scale (Filizola, São Paulo, Brazil). The standing height was measured to the nearest 0.5 cm using a portable stadiometer (Sanny, São Paulo, Brazil) with each subject's shoes off, feet together, and head in the Frankfurt horizontal plane (Lohman, 1986). The body mass index (BMI) was calculated using the standard formula [weight (kg)/height2 (m)]. Triceps and subscapular skinfolds were measured with a Lange caliper (Lange, Santa Cruz, CA). The percent body fat, fat mass (kg) and lean body mass (kg) were estimated using Lohman and Going's formulas (Lohman and Going, 2006).
Physical fitness was assessed according to the standardized tests of the FITNESSGRAM (Research TCIfA 1999) and EUROFIT (1988) batteries, including: (1) handgrip strength (measured independently in each hand) using a handgrip dynamometer (Saehan, Flintville, TN); (2) standing long jump (a measure of the explosive power of the lower limbs); (3) curl-ups (as an indicator of dynamic muscle endurance); (4) sit-and-reach as a measure of flexibility; (5) aerobic fitness (1-mile run/walk test) as an estimate of relative maximal oxygen consumption (VO2max, mL kg−1 min−1) using the equations suggested by a previous study (Cureton et al., 1995); (6) square test as a measure of agility [complete a weaving running course (4 × 4 m2) in the shortest possible time]; (7) and a 20-m run (to evaluate running speed in the shortest possible time).
PA was assessed by a direct interview of each child using the Godin and Shephard questionnaire (Godin and Shephard, 1985). To prevent accuracy problems in reporting their activities, face-to-face interviews were used, and all questions were placed in the children's daily routine contexts. Participants reported the number of times/week that they spent in different activities for a period of at least 15 min. Three PA categories were considered in terms of the metabolic equivalent task (MET) method: mild (3 METs), that is, activities such as easy walking or swimming; moderate (5 METs), that is, activities such as fast walking, leisurely bicycling, volleyball, dance, and noncompetitive swimming; and strenuous (9 METs), that is, activities such as running, jogging, soccer, basketball, judo, roller skating, and vigorous swimming. A total score was derived by multiplying the frequency of each category by the MET value (Godin and Shephard, 1985).
Data quality control
Data quality control was assessed by retesting 10% of the total sample. Intraclass correlation coefficients (R) and respective 95% confidence intervals were used to estimate the relative reliability, the values of which were as follows: height, R = 0.99 (95%CI: 0.98–1.00); weight, R = 0.99 (95%CI: 0.98–1.00); triceps skinfold, R = 0.99 (95%CI: 0.98–0.99); subscapular skinfold, R = 0.99 (95%CI: 0.97–0.99); right handgrip strength, R = 0.98 (95%CI: 0.97–0.99); left handgrip strength, R = 0.98 (95%CI: 0.95–0.99); standing long jump, R = 0.99 (95%CI: 0.96–0.99); sit and reach, R = 0.98 (95%CI: 0.93–0.99); curl-ups, R = 0.95 (95%CI: 0.88–0.98); square test, R = 0.97 (95%CI: 0.89–0.99); 20 m run, R = 0.95 (95%CI: 0.81–0.99); 1-mile run/walk R = 0.88 (95%CI: 0.52–0.97); PA, R = 0.72 (95%CI: 0.61–0.89).
Exploratory data analysis was used to identify possible inaccurate information and the presence of outliers and to test the assumption of normality in all data distributions. Variables with skewed distributions were log-transformed. Descriptive statistics are presented as the means with standard deviations. Interaction factors between sex and age with birth weight were assessed by 2-way ANOVA (i.e., sex × birth weight and age × birth weight). Because no statistically significant interactions were found, data were analyzed as a single group (i.e., boys and girls together). First, group differences between LBW and NBW subjects were examined with independent t-tests. Then, these results were adjusted for age, gender, height, weight, BMI, body composition, and PA using ANCOVA. SPSS 18.0 was used in all analyses, and the level of significance was set at 5%.
Descriptive information regarding body composition and physical fitness is shown in Table 1. The LBW group was shorter, lighter, had lower fat-free mass, and was less physically fit than the NBW group.
|Variables||NBW (n = 256)||LBW (n = 100)|
|Birth Weight (g)||3426 ± 0.2||2084 ± 0.3 a|
|Age (decimal)||8.87 ± 1.0||8.70 ± 1.0|
|Growth and Body Compositions|
|Weight (Kg)b||31.4 ± 7.8||29.4 ± 7.8 a|
|Height (cm)b||133.3 ± 8.4||131.1 ± 8.4 a|
|BMI (Kg/m2)||17.4 ± 3.3||17.1 ± 3.6|
|Body Fat (%)b||21.3 ± 8.4||20.0 ± 8.5|
|Fat Mass (kg)b||7.2 ± 4.6||6.4 ± 4.3|
|Fat-Free Mass (kg)b||24.4 ± 4.6||23.2 ± 4.0 a|
|Sum of triceps and subscapular skinfolds (mm)b||24.4 ± 12.7||22.4 ± 12.5|
|Right Handgrip Strength (kg/f)||14.3 ± 3.5||12.5 ± 3.7c|
|Left Handgrip Strength (kg/f)||13.5 ± 3.6||12.0 ± 3.4c|
|Standing Long Jump (cm)b||109.8 ± 22.4||107.7 ± 21.1|
|Sit and Reach (cm)b||25.3 ± 5.8||24.6 ± 6.0|
|Curl-ups (number of repetitions/min)b||16.4 ± 8.3||15.3 ± 7.6|
|Time to perform a distance in a square with 4 × 4 m (s)||7.6 ± 0.7||7.7 ± 0.6|
|Running speed in 20-m test (s)||4.6 ± 0.4||4.7 ± 0.5a|
|VO2max (mL/kg/min)||45.2 ± 3.7||46.2 ± 3.7a|
|Physical Activity (Mets/15 min/week)b||55.1 ± 23.7||54.9 ± 22.5|
Table 2 presents the adjusted means after controlling for different covariates. The differences in body weight (P = 0.507), height (P = 0.177), and fat-free mass (P = 0.374) disappeared when these means values were adjusted for covariates. Likewise, in aerobic fitness, the differences disappeared when the results were adjusted for gender, height, and fat-free mass. However, the differences in right and left handgrip strength (P = 0.001 and P = 0.006, respectively) and running speed (P = 0.001) remained significant even after controlling for age, gender, height, fat-free mass, and PA.
|Variables||NBW (n = 256)||LBW (n = 100)||Covariates||P-value|
|Growth and Body Composition|
|Weight (Kg)a||30.9 ± 0.02||30.9 ± 0.03||Height, FM, FFM||0.507|
|Height (cm)a||133.0 ± 0.4||131.9 ± 0.7||Age, Gender||0.177|
|BMI (Kg/m2)||17.3 ± 0.09||17.5 ± 0.01||Gender, Age, Fat-Free Mass, Fat Mass||0.353|
|Body Fat (%)a||20.9 ± 0.3||21.2 ± 0.5||Age, Gender, Weight, PA||0.645|
|Fat Mass (kg)a||6.9 ± 0.09||7.1 ± 0.15||Age, Gender, Weight, PA||0.434|
|Fat-Free Mass (kg)a||23.9 ± 0.9||23.8 ± 0.1||Age, Gender, Weight, PA||0.374|
|Sum SE and TR (mm)a||23.7 ± 0.4||24.2 ± 0.7||Age, Gender, Weight||0.605|
|Right Handgrip (kg/f)||14.0 ± 0.15||12.9 ± 0.25b||Age, Gender, Height, PA, FFM||0.001|
|Left Handgrip (kg/f)||13.3 ± 0.16||12.4 ± 0.26c||Age, Gender, Height, PA, FFM||0.006|
|Long Jump (cm)a||108.7 ± 1.1||108.0 ± 1.8||Age, Weight, FFM||0.751|
|Flexibility (cm)a||25.4 ± 0.3||24.4 ± 0.5||Height, FFM||0.139|
|Sit-ups (n/min)a||16.5 ± 0.4||15.1 ± 0.7||Height, Gender, FM||0.113|
|Time to perform a distance in a square with 4 × 4 m (s)||7.6 ± 0.03||7.7 ± 0.06||Height, Weight Gender, FFM||0.177|
|Running speed in 20-m test (s)||4.6 ± 0.02||4.8 ± 0.04c||Gender, Height, FFM||0.001|
|VO2 max (ml/kg/min)||45.3 ± 0.1||45.6 ± 0.2||Gender, Height, FFM||0.312|
Most studies associating the early period of development with later risks of disease have used birth weight as an index of fetal growth, with LBW being shown to be predictive of increased subsequent impairment of health (Barker et al., 2005; Kajantie et al., 2005; Ortega et al., 2009). In this study, we evaluated the short-term influences of LBW in childhood. For body composition, our results showed that LBW children are smaller, lighter, and have less fat-free mass than NBW children. Both groups showed height and weight values within the normal range of the WHO international growth references (de Onis et al., 2006), as well as within the normal range of children from the Northeast of Brazil (Silva et al., 2012). Our findings corroborate previous studies that reported a positive association between birth weight and body weight, height, and fat-free mass during childhood (Chomtho et al., 2008; Kitchen et al., 1992). The consequences of LBW on body composition during infancy can be observed when a remarkable catch-up of growth in weight occurs at adolescence followed by a tendency for obesity and its health risks at adulthood (Saigal et al., 2001). Indeed, the trajectory of growth among children is associated with changes in body composition, mainly a decrease in the skeletal muscle mass and a gradual development of central adiposity (Barker et al., 2005). It seems that LBW children are more susceptible to age-related change in terms of body composition.
In contrast with what was expected for LBW children, our results showed that BMI, %BF, fat mass, and the sum of skinfolds were not different from NBW children. In fact, the association between birth weight and the development of tissues and organs are not the same, and some organs are affected more than others (Wells, 2011). It was interesting to note that LBW children had lower fat-free mass but no changes in body fat. According to the thrifty phenotype hypothesis (Hales and Barker, 1992), tissues may receive more investment to ensure short-term survival associated with the advantages of an immediate alteration in developmental pattern (Hales and Barker, 1992). For example, growth-restricted newborn infants born at or near term retain subcutaneous and intraabdominal adipose tissue compartments to the detriment of lean body mass (Harrington et al., 2004). According to our data, this situation appears to persist during childhood, and a study that follows up LBW children into adolescence would improve the understanding of these associations. Previous longitudinal studies have shown that at adolescence, LBW children have lower growth attainment according to anthropometric parameters and have body compositions associated with a higher prevalence of risk for cardiovascular disease (Hack et al., 1996; Saigal et al., 2001).
By adjusting our results for chronological age, gender, PA levels, and attained body size, our findings were weakened. During childhood, a variety of complementary hormonal processes and environmental factors (diet and PA) may strongly regulate growth and tissue accretion and differentiation (Wells and Stock, 2011). It has been proposed that individuals can present an enough plasticity to adjust their growth and developmental trajectories according to their environments (Wells and Stock, 2011). Recent findings suggest that the nondeterministic implications of perinatal disturbances and children's diversified life histories may attenuate the long-term effects of LBW (Wells, 2010; Wells and Stock, 2011). Herein, we demonstrated that the short-term effects of LBW did not remain after the adjustment for an environmental factor (PA levels) and biological variables (age, sex, body weight, and height).
Our findings concerning the association between birth weight and PA level are in accordance with a previous study wherein the association between birth weight and leisure time PA was very weak within the NBW range (Andersen et al., 2009). Nevertheless, both low and high birth weights are associated with a higher probability to adopt a sedentary lifestyle, which may be a mediator between low PA levels and excessive body weight gain and obesity (Andersen et al., 2009; Rogers et al., 2005).
In the standing long jump, dynamic muscle endurance (curl-ups), flexibility (sit and reach), and agility, LBW children were not significantly different from NBW children. Our findings about physical fitness and birth weight are consistent with reports by other researchers (Ortega et al., 2009; Ridgway et al., 2011; Salonen et al., 2011; Welsh et al., 2010). Explosive force and passive stretch, as measured by the standing long jump, curl-ups, flexibility, and agility tests, did not alter due, as least in part, to the preservation of the passive component of skeletal muscle as observed in prepubertal children (Grosset et al., 2008). To our surprise, LBW children had higher aerobic fitness than NBW children. Aerobic performance is commonly expressed relative to body weight (mL kg−1 min−1), and body weight is negatively associated with endurance performance in running tests (Beunen et al., 1997; Ortega et al., 2009). Additionally, a shorter body stature is associated with a shorter pace, and an increased oxygen cost of running at a given speed and distance (Hebestreit and Bar-Or, 2001).
The most relevant finding of this study is the permanent deficit in muscle strength (handgrip strength) and running speed performance in LBW children even after controlling for covariates. One possible explanation for this reduced muscle performance may be related to a limited metabolic capacity of skeletal muscles as previously described in LBW and ELBW children; these deficits included smaller muscle size, a low proportion of fast-twitch muscle fibers and an impairment in the biomechanical properties of skeletal muscle (Chomtho et al., 2008; Keller et al., 2000; Ortega et al., 2009; Rogers et al., 2006). Our previous study has demonstrated that early malnourished children (9 years ± 6 months) presented lower capacities to develop force under voluntary or induced conditions (Paiva et al., in press). In animals, we previously demonstrated that skeletal muscles might change their phenotype during development in response to perinatal disturbances by changing their contractile and passive mechanical properties (Toscano et al., 2008). If reduced infant fat-free mass is a key mechanism by which LBW leads to low muscle strength and running speed, an important question about the intervention strategies for promoting PA that focus on reaching optimal infant muscle mass, such as physical training, is raised. Our previous studies have shown that moderate physical training attenuated the effects of a perinatal restricted protein diet on the rapid catch-up of growth and reduced fat-free mass in rats during development (Leandro et al., in press; Moita et al., 2011; Pires-de-Melo et al., in press).
In children, LBW alone does not seem to be a major factor that influences body composition and some physical fitness components; however, LBW is a strong predictor of lower performance in muscle strength and running speed tests during childhood. Whether these effects remain into adolescence or adulthood needs to be studied to establish an association between early events in life and later risks of metabolic disease. Because physical fitness is highly responsive to PA level, intervention studies are also necessary to investigate the potential effect of LBW when contrasted with positive environmental stimuli.
The authors' contributions were as follows: M.A.M.S., J.W.B., C.G.L., R.M.C, and M.B.A. designed the study and collected the data; M.A.M.S., C.G.L., and J.A.R.M performed all statistical analyses and wrote the article; all authors were responsible for critical revisions of the article and approval of the final version. The authors thank all the involved children and their families for participating in this study.
- NordNet Study Group. 2009. Birth weight in relation to leisure time physical activity in adolescence and adulthood: meta-analysis of results from 13 nordic cohorts. PLoS One 4: e8192. , , , , , , , , , , , , , , , , , , , ,
- 1991. Exercise performance in very low birth weight children at the age of 7–12 years. Eur J Pediatr 150: 713–716. , , , , , .
- 1999. Early growth and cardiovascular disease. Arch Dis Child 80: 305–307. .
- 2005. Trajectories of growth among children who have coronary events as adults. N Engl J Med 353: 1802–1809. , , , , .
- 1997. Development and tracking in fitness components: Leuven longitudinal study on lifestyle, fitness and health. Int J Sports Med 18 Suppl 3: S171–S178. , , , , , , , , , .
- 2001. Birthweight and aerobic fitness in adolescents: the Northern Ireland Young Hearts Project. Public Health 115: 373–379. , , , , , .
- 2009. Association of 20-year changes in cardiorespiratory fitness with incident type 2 diabetes: the coronary artery risk developmentin young adults (CARDIA) fitness study. Diabetes Care 32: 1284–1288. , , , , , , .
- 2008. Associations between birth weight and later body composition: evidence from the 4-component model. Am J Clin Nutr 88: 1040–1048. , , , , .
- 1995. A generalized equation for prediction of VO2peak from 1-mile run/walk performance. Med Sci Sports Exerc 27: 445–451. , , , , .
- 2006. Comparison of the World Health Organization (WHO) Child Growth Standards and the National Center for Health Statistics/WHO international growth reference: implications for child health programmes. Public Health Nutr 9: 942–947. , , , , .
- EUROFIT. 1988. Handbook for the EUROFIT tests of physical fitness. Rome: Council of Europe Committee for the Development of Sport.
- 2009. Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet 373: 1654–1657. , , , , , , , , , , , , , , , , , , , .
- 2007. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 19: 1–19. , , .
- 1985. A simple method to assess exercise behavior in the community. Can J Appl Sport Sci 10: 141–146. , .
- 2008. Voluntary activation of the triceps surae in prepubertal children. J Electromyogr Kinesiol 18: 455–465. , , , .
- 1996. Catch-up growth during childhood among very low-birth-weight children. Arch Pediatr Adolesc Med 150: 1122–1129. , , .
- 1992. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35: 595–601. , .
- 2004. Distribution of adipose tissue in the newborn. Pediatr Res 55: 437–441. , , , , .
- 2001. Exercise and the child born prematurely. Sports Med 31: 591–599. , .
- 2005. Dynamic soft tissue mobilisation increases hamstring flexibility in healthy male subjects. Br J Sports Med 39: 594–598; discussion 598. , , , , , , .
- 2005. Size at birth as a predictor of mortality in adulthood: a follow-up of 350 000 person-years. Int J Epidemiol 34: 655–663. , , , , , .
- 2000. Anaerobic performance in 5- to 7-yr-old children of low birthweight. Med Sci Sports Exerc 32: 278–283. , , , , .
- 1992. Very low birth weight and growth to age 8 years. I: Weight and height. Am J Dis Child 146: 40–45. , , , .
- 2005. Aerobic and lung performance in premature children with and without chronic lung disease of prematurity. Clin J Sport Med 15: 349–355. , , , .
- 2012. Moderate physical training attenuates muscle-specific effects on fibre type composition in adult rats submitted to a perinatal maternal low-protein diet. Eur J Nutr 51:807–815. , , , , , , , , , .
- 1986. Applicability of body composition techniques and constants for children and youths. Exerc Sport Sci Rev 14: 325–357. .
- 2006. Body composition assessment for development of an international growth standard for preadolescent and adolescent children. Food Nutr Bull 27( 4 Suppl Growth Standard): S314–S325. , .
- 2011. Moderate physical training attenuates the effects of perinatal undernutrition on the morphometry of the splenic lymphoid follicles in endotoxemic adult rats. Neuroimmunomodulation 18: 103–110. , , , , , , , , .
- 2002. Association of maturation, sex, and body fat in cardiorespiratory fitness. Am J Hum Biol 14: 707–712. , , , , , .
- AVENA Study Group. 2009. Are muscular and cardiovascular fitness partially programmed at birth? Role of body composition. J Pediatr 154: 61–66 e1. , , , , , , , , , , ;
- 2012. Stunting delays maturation of triceps surae mechanical properties and motor performance in prepubertal children. Eur J Appl Physiol [Epub ahead of print]. , , , , , , , , .
- 2012. Effects of a moderate physical training on the leptin synthesis by adipose tissue of adult rats submitted to a perinatal low-protein diet. Horm Metab Res 44: 814–818. , , , , , , , .
- 1999. FITNESSGRAM test administration manual, 2nd ed. Champaign, IL: Human Kinetics. .
- 2011. Do physical activity and aerobic fitness moderate the association between birth weight and metabolic risk in youth? the European Youth Heart Study. Diabetes Care 34: 187–192. , , , , , .
- 2006. Associations of size at birth and dual-energy X-ray absorptiometry measures of lean and fat mass at 9 to 10 y of age. Am J Clin Nutr 84: 739–747. , , , , , , , .
- 2005. Aerobic capacity, strength, flexibility, and activity level in unimpaired extremely low birth weight (<or = 800 g) survivors at 17 years of age compared with term-born control subjects. Pediatrics 116: e58–65. , , , , .
- 2001. Physical growth and current health status of infants who were of extremely low birth weight and controls at adolescence. Pediatrics 108: 407–415. , , , .
- 2011. Developmental origins of physical fitness: the Helsinki Birth Cohort Study. PLoS One 6: e22302. , , , , , , , .
- 2012. Growth references for Brazilian children and adolescents: healthy growth in Cariri study. Ann Hum Biol 39: 11–18. , , , , .
- 2003. Programming of lean body mass: a link between birth weight, obesity, and cardiovascular disease? Am J Clin Nutr 77: 726–730. , , , , .
- 2008. Effect of a low-protein diet during pregnancy on skeletal muscle mechanical properties of offspring rats. Nutrition 24: 270–278. , , .
- 2001. Dose-response of physical activity and low back pain, osteoarthritis, and osteoporosis. Med Sci Sports Exerc 33( 6 Suppl): S551–S586; discussion 609–610. .
- 2010. Maternal capital and the metabolic ghetto: an evolutionary perspective on the transgenerational basis of health inequalities. Am J Hum Biol 22: 1–17. .
- 2011. The thrifty phenotype: an adaptation in growth or metabolism? Am J Hum Biol 23: 65–75. .
- 2011. Re-examining heritability: genetics, life history and plasticity. Trends Endocrinol Metab 22: 421–428. , .
- 2010. The EPICure study: maximal exercise and physical activity in school children born extremely preterm. Thorax 65: 165–172. , , , , , , .