What Is Known
- Higher risk of later metabolic disease for those born preterm versus full-term has been reported.
- Rapid growth after hospital discharge in preterm and full-term infants is associated with higher risk of later obesity.
- At term corrected age infants born prematurely have increased adiposity compared with full-term counterparts.
What Is New
- Early differences in body composition between preterm and full-term children resolve by preschool age.
- Infancy fat-free mass gains are associated with preschool lean mass in premature children.
- Close monitoring of body composition (lean vs fat mass) during infancy may allow nutritional support optimization that balances neurodevelopmental benefit and metabolic risk.
Preterm birth is common worldwide, affecting 15 million infants each year according to the World Health Organization (1) and affecting 1 in 9 infants born in the United States in 2012 (2). Overall, reports suggest children born prematurely are at higher risk of later metabolic disease than those born full-term (3). Factors associated with obesity in the infancy time period include infant growth and feeding patterns. Early, rapid weight gain after birth is associated with later-life obesity in those born full-term (4). The same phenomenon is described in those born prematurely, in which greater early weight gain, specifically after term corrected age (CA), has been shown to be associated with later adiposity and obesity in childhood (5), adolescence (6), and adulthood (6–8), and is summarized by Lapillonne and Griffin (9).
Infants born prematurely undergo postnatal growth failure that is disproportionate secondary to linear growth suppression (10–13) and decreased fat-free mass accretion (14,15). This altered growth pattern may be detrimental because it has been related to later neurodevelopment; both linear growth before 12 months CA (11–13) and fat-free mass gains before 4 months CA (16,17) have been associated with improved later cognition. In contrast, increased gains in fat mass have not been associated with improved neurodevelopment. Rather, gains in body mass index (BMI), a surrogate for fat mass based on weight and length or height, are associated with an increased risk of obesity (9,13). Specifically, Belfort et al (13) found that increase in BMI z score during 3 time periods (term CA to 4 months CA, 4–12 months CA, 12–18 months CA) was each weakly to moderately associated with increased risk of overweight or obesity at 8 and 18 years (odd ratios ranged 1.28–2.00 with 95% confidence intervals of 1.02–2.61). There is early evidence that growth in the preterm population during later infancy and childhood, but not convincingly during the neonatal period, is associated with later adverse metabolic outcomes including higher blood pressure and insulin resistance (9). It must be noted, however, that measurement of growth with anthropometrics alone, including BMI, does not accurately reflect body composition—lean mass versus adiposity—for children in general and infants in particular (15,18) and that body composition (eg, fat mass) may be more related to risk of obesity and metabolic disease than weight or BMI alone (19).
Research has not yet established whether body composition tracks from infancy to preschool age in the preterm population. Although there is concern that encouraging rapid growth in the neonatal intensive care unit (NICU) and shortly after discharge could lead to obesity, this has not been reported. Specifically, it is unknown whether or not change in fat-free mass or fat mass during the post-NICU discharge time period is associated with later adiposity. Greater attention in the preterm population to body composition changes (ie, fat and fat-free mass accretion) and adiposity patterns may enable interventions aimed at optimizing the balance between enhancing neurodevelopment and minimizing metabolic risk.
To our knowledge, only 1 prior study has followed a preterm cohort from infancy into childhood with longitudinal body composition measurements (20). They found that weight gain between term and 6 months CA was not associated with fat or fat-free mass at 5 years of age. Their cohort only had body composition measurements at term and at 5 years and therefore they were unable to describe the effect of infancy gains in fat and fat-free mass on later body composition.
The aim of the present study was to characterize changes in body composition from infancy to preschool age in children born prematurely compared to those born full-term, and to test the influence of early gains in fat and fat-free mass on preschool age body composition in both groups. Understanding body composition trajectories in the preterm population may pinpoint when interventions are most likely to alter body composition, obesity, and its downstream metabolic risks.
Twenty-seven premature infants were recruited from the University of Minnesota Masonic Children's Hospital Neonatal Intensive Care Unit between December 2008 and October 2009. Inclusion criteria included gestational age (GA) at birth <35 weeks and appropriate-for-GA (AGA) status (between 10th and 90th percentile on Fenton preterm growth curve (21) at birth). Infants were excluded if they were diagnosed with a clinical condition other than prematurity (eg, chromosomal abnormality, congenital viral infection) known to influence growth. Ninety-seven AGA (between 10th and 90th percentile on World Health Organization growth curve (22)) full-term born infants were also recruited from an on-going study of body composition in healthy infants (23) to be used as a reference population. The University of Minnesota Institutional Review Board approved the initial and preschool follow-up studies, and parents gave written consent for their children's participation.
The infancy findings from the overall study have been previously reported, and further details about the population can be found in that report (14).
Participants were seen for 3 visits in our outpatient research center. Visit 1 occurred near term: after NICU discharge for preterm newborns (38–42 weeks postmenstrual age [PMA]) and approximately 2 weeks after hospital discharge for term newborns (39–44 weeks PMA). Visit 2 occurred in infancy at 3 to 4 months of age, CA for preterms (preterm visits were at 55–62 weeks PMA, term visits were at 50–56 weeks PMA). Visit 3 occurred at 4 years of age, or “preschool age.”
Maternal demographic information including race and highest level of education was collected via self-report at visit 1.
Anthropometrics and Body Composition
Study staff measured anthropometrics and body composition at all 3 visits. Weight was measured on an electronic scale to the nearest 0.1 g. Supine length was measured at Visits 1 and 2 on a length board to the nearest 0.1 cm (Perspective Enterprises Inc, Portage, MI). Standing height was measured at visit 3 to the nearest 0.1 cm using a stadiometer (Seca, Hamburg, Germany).
Body composition was measured via air displacement plethysmography using the PEA POD (COSMED, Ltd.; Concord, CA) for visits 1 and 2 and using the BOD POD with Pediatric Option (COSMED, Ltd) at visit 3. This method has been validated in infants and older children, including those born prematurely, and is described in detail elsewhere (24–27). Briefly, air displacement plethysmography uses measurement of participant weight to the nearest 0.1 g, length or height to the nearest 0.1 cm, and volume to calculate body density. Fat mass and fat-free mass are then derived from body density using the known density of fat along with age- and sex-specific fat-free mass density values, as established by Fomon et al (infancy visits) (28) and Lohman (preschool visit) (29).
Descriptive statistics included means and standard deviations for continuous variables and proportions for categorical variables. To compare between preterm and full-term children, 2-sample t test for continuous variables and Fisher exact test for categorical variables were used.
Two-sample t test was also performed to assess differences in birth weight and GA among those who completed visit 3 and those who did not complete visit 3.
To assess body composition tracking in early life, we tested correlations between infancy (visit 1 and visit 2) measurements and their corresponding measurements at preschool age (visit 3) using partial Pearson correlation coefficients with adjustment for the time interval between the pairs of measurements. Measurements analyzed were fat-free mass, fat mass, percentage (%) body fat, and weight.
To further examine the degree to which neonatal and infancy body composition and relative adiposity predicted preschool body composition, regression analysis was performed. In all models, sex and the time between visits were included as covariates. In addition, as the preterm group was heterogeneous, birth weight and GA were also controlled for in this group. Given the highly correlated linear relation between birth weight and GA (r = 0.91, P < 0.0001) in the preterm cohort, the residuals for each subject (difference between actual and predicted values) of birth weight regressed on GA were used as a single covariate (referred to as “birth weight/GA”). Regression analysis was conducted separately in preterm and full-term groups.
Analyses were performed using SAS system (v9.3; SAS Institute, Cary, NC). Statistical significance was defined at P ≤ 0.05.
Twenty-seven preterm and 97 full-term infants enrolled in the study and were measured at visit 1. Of the original group, 81% of the preterm infants and 54% of term infants were seen at visit 3. A flow sheet detailing the participation and subjects analyzed is found as Supplemental Digital Content 1, Flowchart, http://links.lww.com/MPG/A866. For this manuscript, data on 20 preterm and 51 full-term infants who were seen at all 3 visits are reported.
Compared to those who did not complete visit 3, the preterm infants who were seen at preschool age were slightly larger at birth and born at a later GA; however, these differences were not statistically significant (1843 vs 1327 g, P = 0.06; 31.94 vs 29.86 weeks, P = 0.10). There were no differences in birth weight and GA between the children born full-term who were and were not seen at visit 3.
Supplemental Digital Content 2, Table, http://links.lww.com/MPG/A867, details participant characteristics. Notably, the 2 groups did not differ in sex, race, maternal education, age at visit 3, or BMI at visit 3. The group as a whole does not represent an overweight or obese group at preschool age. Using the United States Centers for Disease Control (CDC) BMI-for-age charts, as recommended for overweight and obesity screening for children 2 to 19 years of age by the CDC and American Academy of Pediatrics, Supplemental Digital Content 3, Table, http://links.lww.com/MPG/A868, describes the prevalence of overweight and obesity in the cohort as defined by BMI percentile (30,31). In summary, 2 children (4%) in the full-term group and 1 in the preterm group (5%) met overweight definition; 3 (6%) in the full-term group and none in the preterm group met obese definition.
Figure 1 depicts mean fat-free and fat mass for each of the groups at visits 1, 2, and 3. Notably, the preterm infants had less fat-free mass and higher adiposity at visit 1 than the full-term children and similar body composition at visit 2, as previously reported (14). Both groups again had similar body composition at visit 3.
Tracking of Body Composition From Infancy to Preschool Age
Table 1 shows the tracking correlations between infancy (visit 1 and visit 2) and preschool (visit 3) measurements. For preterm children there were no statistically significant correlations between visit 1 and visit 3 measurements, but there were moderate correlations between visit 2 and visit 3 for measurements of fat-free mass (r = 0.533, P = 0.019), fat mass (r = 0.532, P = 0.019), and weight (r = 0.748, P = <0.001). In full-term children there were modest correlations between visit 1 and visit 3 fat-free mass (r = 0.304, P = 0.032) and weight (r = 0.291, P = 0.041). There were also modest correlations between visit 2 and visit 3 fat-free mass (r = 0.287, P = 0.044), fat mass (r = 0.354, P = 0.012), and percentage body fat (r = 0.400, P = 0.0040) in full-term children.
Notably, the correlations between infancy and preschool body composition measures were stronger in both groups in later infancy (visit 2) than at the neonatal time point (visit 1). These later infancy correlations were also stronger for preterm than full-term children.
Association of Term/Term Corrected Age Body Composition With Preschool Body Composition
The top section of Table 2 shows the associations of body composition and weight measurements at term/term CA (visit 1) with fat-free mass and adiposity (percentage body fat) at preschool age (visit 3) with further covariate adjustment. For the preterm children, none of the body composition measurements or weight at visit 1 was significantly associated with fat-free mass or adiposity at visit 3. In children born full-term, only visit 1 fat-free mass was associated with visit 3 fat-free mass (β = 1.41, R 2 = 0.15, P = 0.018), and the association was weak.
Association of Infancy Body Composition Changes With Preschool Body Composition
The bottom section of Table 2 shows the associations of rates of change in body composition and weight measurements from term/term CA to 3 to 4 months/3 to 4 months CA (visit 1 to visit 2) with fat-free mass and adiposity (percentage body fat) at preschool age (visit 3) with further covariate adjustment.
Fat-free mass gains (grams per week) from visit 1 to 2 were significantly associated with visit 3 fat-free mass (kg) in preterm children (β = 0.038, R 2 = 0.50, P = 0.049) but not full-term children (β = 0.009, R 2 = 0.08, P = 0.19). Each gram of fat-free mass gained per week from visit 1 to visit 2 in the preterm children was associated with an increase of 38 grams of fat-free mass (SE 0.018) at Visit 3. None of the other measured changes were associated with visit 3 fat-free mass in either group.
Gains in both adiposity measurements (fat mass, g/week, and % body fat, %/week) from visit 1 to 2 were significantly associated with visit 3 adiposity (% body fat) in the full-term but not preterm children. Change in weight (g/week) over the same time period was positively associated with visit 3 adiposity; the relation was significant in the full-term group (β = 0.032, R 2 = 0.21, P = 0.0068) and neared significance in the preterm group (β = 0.107, R 2 = 0.31, P = 0.052). Changes in fat-free mass between infancy visits were not associated with visit 3 adiposity in either group.
Although many studies have found that preterm and term infants have differences in body composition at term (14,15), reported timing of resolution of these differences has varied widely between groups (20,32–34). We report that despite early differences in body composition between term and preterm infants in our cohort, these differences were resolved by 3 to 4 months CA (14) and that body composition remained similar in the 2 groups when measured at preschool age. Despite the potentially short-lived differences, the long-term implications of these early growth alterations are largely unknown. This is the first study to compare the relation between early postdischarge changes in body composition and preschool body composition in preterm and full-term infants. We found that early neonatal measurements (visit 1) were not correlated, whereas infancy measurements (visit 2) were correlated with preschool measurements (visit 3) in the preterm group. We then specifically showed that early fat-free mass accretion over the first 3 to 4 months after term CA is significantly associated with increased fat-free mass at preschool age for the preterm group.
We previously reported that preterm infants at term CA had less fat-free mass and higher adiposity when compared to full-term counterparts (14). These findings have been replicated by several other groups, as reported in Johnson's meta-analysis (15). Our group also previously reported, on this group of infants, that body composition was similar by 3 to 4 months CA (14), whereas others have reported lower amounts of fat mass in preterm infants at 3 months CA (35).
Fewer studies have compared childhood body composition between preterm and full-term children. Darendeliler et al (33) reported similar body composition in AGA preterm and full-term children approximately 4 years of age as measured by dual-energy x-ray absorptiometry. In contrast, Huke et al (34) reported that AGA preterm children had lower body fat index (fat mass [kg]/height [m]2) compared to full-term counterparts at early school age as measured by bioelectrical impedance analysis. The mean GA (29.8 weeks) and birth weight (1434 g) in the latter group were lower than our study, and thus may represent a smaller and likely sicker population than ours. Both studies also differ in the method used for body composition measurement.
Ours is the second longitudinal report of premature children's body composition and the only study with more than 2 data points. The first report by Gianni et al described a cohort of 124 children born premature and full-term who had body composition measured around term or term CA and at 5 years of age via air displacement plethysmography (20). They found that boys born prematurely had lower fat-free mass at 5 years of age compared with full-term counterparts (20). Because of our small sample size, we did not compare boys and girls separately but included sex as a covariate in the analysis to control for known sex differences in body composition. The preterm participants in their study included only children born very low birth weight (VLBW, <1500 g), 27% of whom were born small-for-gestational-age. It is not surprising that our findings differ slightly given the differences in the 2 study populations. There are known differences in body mass accretion between small-for-gestational-age and AGA infants (36,37). In addition, given their population of all VLBW infants, there are also likely differences between the 2 study populations in early exposure to illness and nutritional deficiencies known to influence body composition (14,38,39).
Fewtrell et al (32) reported differences in school-age body composition showing lower body fat index at 8 to 12 years of age measured by skin folds and/or dual-energy x-ray absorptiometry in those born preterm versus full-term controls. The preterm population in that study had similar birth weight and GA to our study, however, was born in the early 1980s when nutritional practices and clinical care were likely quite different from current standards. In addition, body composition accretion may again diverge from the full-term population at some time point after preschool age. Continued attention to the progression of longitudinal body composition changes in this population, measured at multiple time points, is certainly prudent.
This is the first analysis of associations between infancy and preschool body composition in the preterm population; whether or not body composition tracks from infancy to early childhood in this population has not been established. Despite having greater relative adiposity at term CA than their full-term counterparts, the preterm infants’ body composition at term CA (visit 1) was not significantly associated with adiposity at visit 3. Evidence linking both optimal early nutrition (9,40) and improved growth (11,17,41–43) before term CA with long-term neurodevelopment is strong. Together these findings and ours suggest that optimizing nutrition and growth early on, before term CA, may allow for improved neurodevelopment without increasing risk of later overweight or obesity.
There is concern that encouraging rapid growth and weight gain both in the NICU and shortly thereafter may lead to later obesity. More rapid length and BMI gains from term to 4 months CA and more rapid weight gain in the first year of life have been shown to incur higher risk of overweight and obesity in childhood and adolescence (5,13). Rapid growth in the NICU is, however, critical for neurodevelopment as demonstrated in large studies (41,42). It remains unclear whether that rapid growth in preterm infants incurs the same metabolic risk as it does in term infants (6,7,9,13,43). In regards to metabolic outcomes, our findings suggest the period of growth that deserves attention is postdischarge, given that early infancy (visit 2) but not neonatal/term CA (visit 1) measurements were significantly correlated with respective measurements in early childhood (visit 3), as summarized in Table 1.
Our findings also suggest that lean mass gains during the term to 4 months CA infancy time period are associated with lean mass at preschool age. In this group of preterm children, the only association (nearing significance) with increased preschool adiposity (visit 3) was overall weight gain during the infancy time period (visit 1 to visit 2) and not changes in body composition. This is in contrast to the full-term group for whom gains from visit 1 to 2 in both weight and adiposity (fat mass and percentage body fat) were associated with increased % body fat at preschool age (visit 3), as previously reported (44,45). Targeting fat-free mass over fat mass accretion in early infancy may be protective against later adiposity in the preterm population, although overall weight gain likely should not be ignored.
As noted, our study population was not, on average, overweight or obese at preschool age per the BMI definition from the CDC and American Academy of Pediatrics (30,31). The association of increased infancy weight gain with increased preschool adiposity may, however, be a risk factor for later overweight or obesity and other adverse metabolic outcomes. Also, our study did not investigate other important metabolic outcomes such as insulin resistance and hypertension. Certainly, larger studies in the preterm population among different groups or stratified by birth weight and GA are needed to clarify the effect of early growth on long-term adiposity and metabolic risk outcomes.
These novel data, although early and exploratory, have important clinical implications as neonatologists work to strike a balance between optimizing neurodevelopment and minimizing later metabolic risk. We speculate that increased adiposity at preschool age may precede later overweight, obesity, and other metabolic consequences, although our study does not establish this; longer follow-up is needed. In particular, the postdischarge time period remains an important epoch of growth to investigate, because neonatologists and primary care providers continue to control nutritional intake after term CA, albeit less so than during NICU hospitalization, through fortification of feedings. Our present study suggests that over this time period fat-free mass gain is associated with later fat-free mass whereas weight gain is associated with later adiposity, but it is unable to delineate if there is an ideal balance between lean compared with fat mass gains. Of note, fat-free mass gains during the postdischarge period have been associated in preterm infants with improved speed of processing, a potential surrogate for later neurodevelopment (16). Practices in fortification vary widely, and there is little data on the long-term effects of these nutritional supplements (43,46–49). To our knowledge there is only 1 study that has investigated postdischarge fortification regimens targeting an enhanced balance of fat-free mass over fat mass gains. Roggero et al (50) reported that infants fed more protein via preterm formula had increased fat-free mass gains with decreased relative adiposity after 6 months of supplementation. Future larger studies investigating body composition changes in preterm infants fed human milk with various postdischarge fortification regimens that examine both enhancing neurodevelopment and reducing metabolic risk will be important to establish optimal growth patterns.
Our study is limited by its small sample size, heterogeneity of the preterm group in regards to birth weight and GA, and the low follow-up rate for the full-term group at visit 3 (although birth characteristics were not different between those seen or not at visit 3). Also, the preterm group seen in follow-up included fewer VLBW infants than the original sample. Thus, selection bias toward larger and healthier preterm infants may have been introduced. Given the overall heterogeneity of the preterm group and possible selection bias at visit 3, readers are cautioned from drawing conclusions for particular groups of preterm infants. Despite the limitations, it is the first longitudinal study in this population documenting the tracking of infancy to early childhood body composition and the association of early infancy growth with early childhood body composition. Given the small sample size we were unable to control for additional covariates of neonatal factors known to influence body composition including NICU nutrition and illness in the preterm group and on-going factors of nutrition, physical and sedentary activity, and sleep in both groups. Future studies with larger sample sizes should certainly give attention to these factors. Lastly, although early infancy is an important period of growth to examine, there are likely other important and critical periods of growth between 4 months CA and preschool age that have an influence on metabolic outcomes. We were unable to examine those time periods given the schedule of the 3 visits.
In conclusion, the present study reports serial associations of body composition from early infancy to preschool at 3 time points and their differences in children born premature versus full-term. For preterm children only infancy fat-free mass gains were significantly associated with increased preschool fat-free mass. Larger studies in this population with additional time points of serial anthropometric and body composition measurements are needed to establish optimal growth patterns aimed to balance the potentially opposing metabolic risks and cognitive benefits. Future nutritional intervention trials should include both long-term neurodevelopmental and metabolic outcome measures.
The authors wish to thank the study participants, families, and staff; The Benjamin Walker Hanson Fund of the University of Minnesota Foundation and the Center for Neurobehavioral Development for financial and logistical support; Dr Michael Georgieff, Head of Division of Neonatology, for critical appraisal of the study design and assistance with statistical analysis and interpretation; and The Biostatistical Design and Analysis Center of The Clinical and Translational Science Institute of the University of Minnesota for performing statistical analysis.
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