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Original Articles: Hepatology and Nutrition

Optimal Growth and Lower Fat Mass in Preterm Infants Fed a Protein-enriched Postdischarge Formula

Amesz, Eline M*; Schaafsma, Anne; Cranendonk, Anneke*; Lafeber, Harrie N*

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Journal of Pediatric Gastroenterology and Nutrition: February 2010 - Volume 50 - Issue 2 - p 200-207
doi: 10.1097/MPG.0b013e3181a8150d
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Many preterm-born infants develop postnatal growth retardation in the first weeks after birth (1,2). Impaired postnatal growth is associated with poorer cognitive outcome; therefore catch-up growth is presumably beneficial for the neurodevelopment of these infants (3). To enhance this catch-up growth, preterm infants, who are on an average between −1 and −2 standard deviation score (SDS) for body weight at term age (corresponding with 40 weeks postconceptional age), have been fed special formulas with extra energy and/or protein in the first weeks to months after discharge. The results of studies examining the effects of these formulas have not been consistent, and it has been concluded that there is no strong evidence that postdischarge formula (PDF) compared with the standard term formula affects growth rates or development up to 18 months postterm (4–8). However, a recent article compared feeding preterm formula or term formula (TF) after term during 2 months and showed better growth and mineralization (9).

In recent years, it has also become clear that a period of rapid growth may have negative effects on long-term health outcome (10). Unbalanced catch-up growth of fat mass (FM) could be attributing to this association. Rapid early weight gain in preterm-born infants has been associated with a higher fat percentage and a more abdominal fat distribution at young adult age (11). The composition of formulas is known to influence body composition. Excessive nonprotein energy is stored as fat independently, if it is energy supplied by carbohydrates or fat (12). Formula with a higher protein-to-energy ratio has been associated with increased gain of lean mass (LM) (13,14).

It is not clear until what age growth, body composition, and neurodevelopment of preterm-born infants can be influenced with protein- and/or energy-enriched nutrition. Infants were primarily randomized to these formulas or standard formula at discharge from the hospital, usually at a mean gestational age of 36 to 37 weeks. Two studies examined the effect of protein- and energy-enriched nutrition after term corrected age. Results of these studies suggest that growth and neurodevelopment can not only be improved with protein and energy enriched nutrition between discharge from the hospital and term corrected age but also thereafter (15,16). Only 1 of these studies considered quality of growth, and no differences in weight gain composition were observed (16). However, in that study the beneficial effect of a higher protein-to-energy ratio may have been undone by increased fat storage because of the high level of energy in the studied protein- and energy-enriched formula.

We hypothesize that differences in growth and weight gain composition will develop between preterm infants fed nutrient-enriched PDF without extra energy or standard formula between term and 6 months corrected age. Infants who received unfortified human milk after term corrected age were used as a reference group.



The present prospective, controlled, and randomized study was approved by the Ethics Committee of the Vrije Universiteit Medical Centre (VUMC) and informed consent was obtained from the parent(s). All of the infants were recruited from 1 neonatal unit (VUMC, Amsterdam, the Netherlands) between 2003 and 2006, with 6-month follow-up completed in December 2006. Infants with a gestational age less than or equal to 32 weeks or with a birth weight less than or equal to 1500 g were considered eligible for the study if 1 of their main caretakers spoke Dutch or English. Infants with congenital malformations or conditions known to affect growth and/or body composition (eg, severe bronchopulmonary dysplasia, inborn error of metabolism, cardiac or renal disease, necrotizing enterocolitis with substantial gut loss, grade IV intraventricular hemorrhage) were not included.

Study Design

Until term corrected age infants were fed human milk, or if that was not (sufficiently) available, a standard preterm formula was given (Table 1). Human milk was fortified with standard breast milk fortifier until term corrected age (corresponding with postconceptional age 40 weeks). Infants receiving unfortified human milk were supplemented with 200 IU of vitamin D daily. At term corrected age (40 weeks postconceptional age nonbreast-fed infants were randomized to a standard TF (Friso 1 normaal, Friesland Foods, Leeuwarden, the Netherlands) or a nutrient-enriched PDF (Friso 1 premature, Friesland Foods) and remained on that formula until 6 months corrected age. The composition of the study formulas is shown in Table 1. The PDF provided the same quantity of energy but a higher level of protein and a lower level of carbohydrates, higher levels of some minerals, vitamins, and long-chain polyunsaturated fatty acids (DHA/AA) per 100 mL than the TF. Both formulas were supplied by Friesland Foods. Infants fed their own mother's milk, supplemented or replaced by standard formula if necessary, were regarded to be exclusively human milk fed as long as human milk was at least 80% of the total milk intake. Supplements providing additional energy were limited as much as possible before term corrected age and were not allowed thereafter. Parents were asked not to introduce any other food until their infants were 5 months' postterm and to limit the food introduced to fruits and vegetables.

Composition of the trial formulas

An independent researcher used a computer-generated randomization table provided by Friesland Foods that was stratified for sex to assign infants for feeding with treatment A or B. This corresponded with batch numbers on the nutrition products that were otherwise identically labeled. Investigators, parents, and medical and nursing staff were unaware of treatment allocation. Primary outcome of the randomized trial (nutrition A or B) was the power to detect a 500-g (±0.5 SD) difference in weight at 6 months corrected age, a 300-g difference in LM, and a 3% difference in fat percentage at 6 months corrected age at 5% significance and 70% to 80% power (6,16). To that end each group should have a sample size of at least 45 infants. This sample size was determined before the study was started. Because it was suggested by the European Society for Paediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN) nutrition committee that in particular preterm infants who have a negative SDS for weight at 40 weeks postconceptional age (17) may benefit from postdischarge nutrition, a subgroup analysis was made after the study had been completed creating arbitrarily chosen subgroups of formula-fed infants that were above or below −1.3 SDS for weight at postconceptional week 40.

Obstetric data, clinical progress, growth, and intake until discharge were collected from hospital records by a single person. After discharge, parents kept weekly diaries considering growth and intake. In addition, these topics were discussed during telephone calls performed by a single person every 1 to 2 weeks. Infants were seen by an experienced research nurse at the outpatient clinic at term, 3, and 6 months corrected age, respectively. At each clinical visit infants were weighed nude on a digital electronic scale, length was measured using a length board, and head circumference was measured using a nonstretchable measuring tape. A venous blood sample was obtained at least 2.5 hours after feeding and serum level of urea nitrogen was determined (enzymatic kinetic assay [Roche Diagnostics, Mannheim, Germany], interassay coefficients of variation 1.9%). Body composition was measured by DEXA (Hologic QDR 4500A, Hologic Inc, Bedford, MA) at term and 6 months corrected age. The use of this fan-beam DEXA in small subjects has been described before (18,19). Daily calibration was performed by scanning the phantom swaddled in an infant cotton sheet, the scanning area covered with plastic material, as with the scanning of the infants. Coefficients of variation were 2.3% for LM and 5.4% for FM. Scans were usually performed just after a feed and were started when the infant was settled. The research nurse was constantly in attendance. Scan analysis was performed with Infant Whole Body Software, version 12.3.3. Scans with severe movement artifacts as described by Koo et al (20) were excluded from analysis.

Weight and length were expressed as SDSs with the use of Swedish references for very preterm infants at birth and term (21), and with the use of Dutch reference values at 3 and 6 months corrected age (22).


Results are presented as mean ± SD or median (interquartile range) if variables were not normally distributed. Not-normally distributed data were transformed with square root, logarithm, or inverse function before statistical comparison. If transformation did not adequately improve distribution, non-parametric tests were used. Differences between the 2 formula groups were compared by unpaired t test, Mann-Whitney U test, or χ2 test. Differences between infants in the formula groups and infants fed human milk were compared using analysis of variance, with post hoc analysis using Dunnett test, Kruskal-Wallis test, or χ2 test. To correct for other factors of influence, an analysis of covariance was also conducted for differences in body composition between the 2 formula groups. LM without bone mineral content was used for analysis. Both LM (kg) and FM (kg) were adjusted for height (m) to calculate the lean (fat free) mass index (FFMI) and the fat mass index (FMI) as follows: FFMI = LM/height2 and FMI = FM/height2(23,24). Gain in LM and FM was calculated as the difference between the 2 DEXA scans divided by the weight calculated by DEXA at 6 months corrected age and the number of days between the 2 scans.

Analyses were performed with the use of SPSS version 12.0.1. Statistical significance was defined as a P value less than or equal to 0.05.


Of the 152 infants participating in the study, 102 infants were randomized at corrected term age (corresponding with 40 weeks postconceptional age) to 1 of the 2 trial formulas, whereas the mothers of 50 infants indicated that they intended to continue breast-feeding. Of the 102 randomized infants, 93 infants completed the study at 6 months corrected age (Fig. 1). Of the TF infants, 2 infants were excluded because of severe bronchopulmonary dysplasia with failure to thrive, 2 infants because of an inborn error of metabolism, 2 infants did not get the study formula at the right time, and 3 infants were withdrawn from the study by their parents. Body composition data both at term and at 6 months corrected age in 43 infants in the PDF group and 34 infants in the TF group were taken because data of 9 infants (PDF) and 16 infants (TF) were not available due to movement artifacts at term corrected age, as described by Koo et al (20). Fifty infants were exclusively fed human milk until term corrected age, 19 infants at 3 months corrected age, and 7 infants even at 6 months corrected age. Until the postconceptional age, that is 40 weeks, 89% of these infants received breast milk fortifier. From the exclusively human milk–fed infants, body composition data were available at term from 24 infants, at 3 months corrected age from 19 infants, and at 6 months corrected age from 7 infants (Fig. 1). Characteristics of the infants are shown in Table 2. There were no differences in characteristics or body size between infants who were excluded from body composition analysis because of movement artifacts on the scans and infants who were included in the analysis.

Flow diagram of infants included in the study. DEXA = dual energy X-ray absortiometry; HM = human milk; PDF = postdischarge formula; PTF = preterm formula, TF = term formula.
Characteristics of the infants

Volume and energy intakes were not different between infants in the PDF and the TF groups (mean intake PDF 170 ± 20 mL kg−1 day−1, TF 169 ± 13 mL kg−1 day−1, 3 weeks after term). As expected, infants fed PDF had higher protein intakes than infants fed TF (4 weeks corrected age 2.84 ± 0.32 vs 2.51 ± 0.35 g kg−1 day−1, P < 0.001; 8 weeks corrected age 2.82 ± 0.34 vs 2.45 ± 0.29 g kg−1 day−1, P < 0.001; and 16 weeks corrected age 2.48 ± 0.39 vs 2.16 ± 0.39 g kg−1 day−1, P < 0.001).

In all of the infants the weaning process could be postponed until corrected age 5 months. During the period of 5 to 6 months corrected age weaning foods were introduced such as porridge made out of grain, sunflower, or rice. In most cases, bread was also introduced during this period.

Serum urea nitrogen was 4.7 ± 1.2 mmol/L at term corrected age, 3.9 ± 2.0 mmol/L at 3 months, and 2.8 ± 0.2 mmol/L at 6 months corrected age in all groups, with no significant differences between the PDF- and TF-fed groups.

There were no differences between the feeding groups in standard deviation scores of weight, length, and head circumference or in body mass index at term, 3, and 6 months corrected age (Fig. 2). Gain in weight, length, and head circumference was also not significantly different, although differences between infants fed formula and infants fed human milk were sometimes more than or equal to 0.5 SD (Table 3). In terms of absolute LM and FM there were no differences between infants in the PDF and TF groups (Table 4). However, after correction for body size, infants in the PDF group had a lower FM at 6 months corrected age than infants in the TF group. Both FM corrected by weight (FM percentage) as FM corrected by height (FMI) were lower in the PDF group than in the TF group. In addition, infants in the PDF group gained most LM and less FM between term and 6 months corrected age than infants in the TF group. Body size at 6 months corrected age was associated with body size at birth and at term corrected age, and with growth between birth and term and term and 6 months corrected age. Weight gain composition was also associated with these factors. Differences in body composition and weight gain composition between the formula groups remained significantly different if these influences were taken into account (ANCOVA PDF vs TF FMI at 6 months corrected age P = 0.020, FM percentage at 6 months corrected age P = 0.036, gain LM P = 0.027, gain FM P = 0.008).

Between the various SDS values and between the BMI values there were no significant differences. •, PDF = postdischarge formula; •, TF = term formula; ♦, HM = human milk fed exclusively until 3 months corrected age; ⋆, HM fed exclusively until 6 months corrected age. BMI = body mass index; SDS = standard deviation score.
Gain in weight, length, and head circumference between term and 6 months corrected age expressed as SDS
Body composition and body composition corrected for body size in the complete group

After post hoc subgroup analysis of infants under or above −1.3 SDS at term corrected age (as described above), differences in body composition corrected for body size and weight composition were seen among boys but not among girls (Table 5). Because it was suggested by the ESPGHAN nutrition committee that in particular preterm infants who have become malnourished at term age may benefit from postdischarge nutrition (17), specific subgroup analyses were made in preterm infants with a weight SDS less than −1.3 at term and in those with a weight SDS more than or equal to −1.3 SDS at term. These analyses showed that differences in body composition between the formula groups reached significance among infants with a weight SDS less than −1.3 at term but not among infants with a weight SDS more than or equal to −1.3 at term.

Fat mass corrected for body size and weight gain composition for the group separated by gender or by weight SDS at term

Infants exclusively fed human milk until 6 months corrected age gained less LM and more FM than infants in the PDF group and had lower LM than infants in both the formula groups at 6 months corrected age (Table 4). After correction for body size, this difference in LM at 6 months corrected age between infants fed formula or human milk remained; FM corrected for body size at that age was also higher in infants fed human milk than in infants in the PDF group.


This randomized controlled trial shows that although quantity of growth is not different, weight gain composition is different between preterm infants fed a nutrient-enriched formula without extra energy or a standard formula between term and 6 months corrected age. As a result, infants fed this specific enriched formula after term have a lower FM corrected for body size at 6 months corrected age than infants fed a standard formula. A limitation in our study is the fact that for power analysis it was assumed that least 45 infants were included in every arm. However, over time infants were lost for analysis in particular because of movement artifacts in the DEXA scan at 0 and 6 months corrected age (Fig. 1).

Results of studies examining the effect of postdischarge nutrition on growth of preterm infants after discharge have been inconsistent. This is probably because of heterogeneity in formula composition (energy-enriched or not, amount of extra protein, and protein-to-energy ratio), duration of formula feeding, and inclusion criteria. In a Cochrane review, it was concluded that there is some evidence that growth improves with energy- and protein-enriched formula after discharge; however, the authors emphasized that the clinical significance of these small differences in growth is unclear (8). In a more recent randomized controlled trial infants fed standard formula showed improved growth compared with infants fed enriched formula (25). Some studies examined the effects of a protein-enriched formula without extra energy after discharge. Wheeler and Hall (7) found a beneficial effect on gain of length and head circumference, but Koo and Hockman (25) observed no significant differences in growth. In both of the studies the enriched formula contained a little bit more protein (1.83 g/100 mL) and thus had a higher protein-to-energy ratio than the nutrient-enriched formula in our study and infants were randomized on average 3 to 4 weeks earlier.

Agosti et al (15) and Cooke et al (5) have examined the effect of randomizing preterm infants to enriched or standard nutrition at term corrected age. Both studies used formulas with extra energy and protein. In the study of Cooke et al (5), 2 formulas were enriched with different amounts of both protein and energy, differences in growth were seen in boys and infants that were small for gestational age at birth. In the study of Agosti et al (15), 1 group of infants continued to receive a energy- and protein-enriched formula after term and the other group received standard formula after term. Again differences in growth were seen in boys. These studies demonstrate that it is possible to influence quantity of growth of preterm infants with energy- and protein-enriched nutrition after term corrected age. Recently, a study by Picaud et al (9) continuing feeding a preterm formula for 2 months after discharge in comparison with a TF showed better growth and mineralization 4 months after growth.

The results of our study suggest that an increase of the protein-to-energy ratio to 2.54 g/100 kcal after term corrected age, without addition of extra energy, does not affect the quantity of growth but has an impact on the quality of growth. However, because the sample size of the post hoc subgroups analysis was limited, it cannot be ruled out that certain subgroups of infants do benefit from an increase of the protein-to-energy ratio to 2.54 g/100 kcal after term corrected age. This needs to be analyzed in further studies.

No differences were seen in body mass index, contrary to the observed differences in body composition measured by DEXA. Body mass index, however, does not distinguish between FM and LM, as has been argued before (24). Fan-beam DEXA has been validated to measure body composition in small subjects accurately and precisely (18,19). Commercial software, however, may overestimate FM and underestimate LM, with inaccuracies increasing when subjects weigh more (27). Therefore, only comparisons between infants with comparable body weights were made. Fat mass percentage is not an independent measure of body fat corrected for body size because it is dependent on LM; therefore, it has been recommended to adjust FM and LM for height to create independent measures (23,24). With these independent measures it can be determined whether a higher FM percentage is because of less LM, more FM, or both. In the present study, LM expressed as a percentage of weight, a measure often used before, would have been significantly higher in the PDF than in the TF group at 6 months corrected age (74.6 ± 7.2 vs 71.4 ± 6.3, P = 0.050). However, LM and FM corrected for height (lean mass index [LMI] and FMI), showed that the decreased FM percentage in the PDF group was the result of less FM, and not due to any differences in LM.

Three out of 4 other studies evaluating the effects of nutritional intervention after discharge on body composition of preterm infants by DEXA, found an effect on body composition (14,16,25,26). In the study of Brunton et al (14) both formulas were energy enriched, infants fed the formula having higher protein-to-energy ratio had a higher absolute LM and lower FM percentage. In the study of Koo and Hockman (25), absolute lean and FM were increased in infants fed the standard formula, but FM percentage was lower in infants fed the energy- and protein-enriched formulas. Furthermore, in the study of Cooke et al (16) absolute lean and FM were higher in the group of infants that received the energy- and protein-enriched formulas, but there were no differences in FM percentage. In the fourth study, no differences in body composition or weight gain composition between the feeding groups were seen; growth restriction at discharge, however, did seem to have an effect on weight gain composition (28).

Our observed differences in body composition between formula-fed infants and infants fed human milk are in agreement with the results of other studies comparing the effect of human milk and formula feeding on body composition in infancy in term (29) and preterm (30) infants. In term infants these differences seemed to be temporary, but in preterm infants they were still present at a corrected age of 1 year. Whether supplementation of human milk with extra protein or fortifier after term would influence body composition of preterm infants fed human milk remains an interesting question.

Subgroup analysis revealed that differences in body composition developed predominantly among male infants. Because the ESPGHAN nutrition committee recommended that specifically infants with a subnormal weight at discharge should be fed enriched formula after discharge (17), another subgroup analysis was performed. The results of this analysis support the advice of the ESPGHAN nutrition committee, because the differences between the 2 formula groups among infants with a weight SDS less than −1.3 at term were highly significant, and no differences were seen among infants with a weight SDS more than or equal to −1.3 SDS at term. Other studies also found that especially male infants and the smallest infants benefit from enriched postdischarge nutrition (4,6,16). However, it is clear that there are limits to the creation of several subgroups of growing or not growing preterm infants that may or may not benefit from a certain diet composition, leading eventually to a tailor-made composition of formula for each individual infant. The decision as to whether certain subgroups of infants should and other subgroups of infants should not be given enriched formula after discharge should be taken after various (neurological) outcomes have been considered.

It is not known whether differences in body composition at this young age will persist at an older age or will have any long-term health consequences. However, preterm birth probably is a risk factor for decreased insulin sensitivity (31), and a combination of low birth weight SDS and increased absolute FM and FM percentage has been associated with increased insulin resistance in adults who were born preterm (32).

The PDF used in the present study was specifically enriched with extra protein, but also contained higher levels of long-chain polyunsaturated fatty acids, calcium, and phosphate. It is therefore not possible to conclude which of these nutrients causes differences in weight gain composition. Other studies have concluded that a higher protein-to-energy ratio is associated with improved LM gain; however, the amount of long-chain polyunsaturated fatty acids in the diet has also been associated with differences in weight gain composition (33).

In conclusion, the present study shows that differences in weight gain composition and in body composition develop, without changing the quantity of growth, when preterm infants are fed a nutrient-enriched formula without extra energy instead of a standard formula after term corrected age. Infants fed this specific PDF had lower FM corrected for body size at 6 months corrected age than infants fed standard formula or human milk. Especially male infants and infants with a weight SDS less than −1.3 at term seem to benefit. Whether the observed differences in body composition will persist at an older age and whether differences in weight gain composition can be enlarged by further increasing the protein-to-energy ratio and/or the amount of energy needs to be further investigated.


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body composition; enriched formula; growth; infant formula; postdischarge nutrition; premature infant

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