European Journal of Clinical Nutrition (2014) 68, 12611263

2014 Macmillan Publishers Limited All rights reserved 0954-3007/14

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SHORT COMMUNICATION

Lean mass and fat mass accretion between term age and
6 months post-term in growth-restricted preterm infants
M van de Lagemaat, J Rotteveel, HN Lafeber and MM van Weissenbruch
Early growth restriction followed by nutritional intakes that permit accelerated growth may result in adiposity and metabolic
disease in later life. This study compared growth, body composition and nutritional intake between term age and 6 months postterm in 83 appropriate-for-gestational-age preterm infants with growth restriction at term age (AGA GR+), 15 AGA without growth
restriction at term age (AGA GR ) and 33 small-for-gestational-age (SGA) preterm infants. AGA GR+ and SGA preterm infants had
higher protein intake, higher energy intake and higher gain in weight SDS between term age and 6 months post-term, with similar
lean mass (LM) and lower fat mass (FM) at 6 months post-term compared with AGA GR preterm infants. In conclusion, despite
higher energy and protein intake compared with AGA GR preterm infants during the rst 6 months post-term, AGA GR+ and SGA
preterm infants restore their LM without excessive FM.
European Journal of Clinical Nutrition (2014) 68, 12611263; doi:10.1038/ejcn.2014.182; published online 17 September 2014

INTRODUCTION
Growth without increased fat mass (FM) accumulation may be
especially important for infants who are prone for accelerated
growth during infancy, such as preterm infants born appropriatefor-gestational-age (AGA) with growth restriction before term age
(AGA GR+) and small-for-gestational-age (SGA) preterm infants.1,2
Accelerated infant growth is associated with adiposity and
metabolic consequences in later life, and may be related to
nutritional intakes.3,4 The present study compared growth, body
composition and nutritional intake until 6 months post-term
between AGA preterm infants with and without growth restriction
at term age (AGA GR+ and AGA GR , respectively) and SGA
preterm infants.
SUBJECTS AND METHODS
This study was part of a trial on postdischarge nutrition5 and
included 83 AGA GR , 15 AGA GR+ and 33 SGA preterm infants.
At birth, term age and 6 months post-term, weight (g) and length
(cm) were measured and expressed as standard deviation scores
(SDS).6,7 Infants were classied as AGA GR (weight and length at
birth and term age 2 SDS), AGA GR+ (weight and length at
birth 2 SDS and weight, length or both at term age o 2 SDS)
and SGA (weight, length or both at birth o 2 SDS).1,8 Energy
(kcal/kg/day), protein (g/kg/day), fat (g/kg/day) and carbohydrate
intakes (g/kg/day) were calculated in formula-fed infants between
term age and 6 months post-term based on data from the infants
medical record and parental diaries. Lean mass (LM; g) and FM (g)
were measured by whole-body dual-energy X-ray absorptiometry
(Hologic QDR4500A, Hologic, Bedford, MA, USA) at term age and
at 6 months post-term and analyzed by Infant Whole Body
Software version 12.3.3.5 Gain () in weight and length SDS and
LM and FM between term age and 6 months post-term were
calculated. Statistical analyses were performed with SPSS 17.0 for

Windows (SPSS, Chicago, IL, USA). Parameters were compared

between groups by regression analysis with the between-group
comparisons as dummy variables, adjusted for gender and
gestational age. Differences between groups were not explained
by type of diet and severity of illness. A (two-sided) P-value of 0.05
was considered signicant.
RESULTS
SGA infants were more often boys than AGA GR and AGA GR+
infants (73% versus 43% and 40%, P o0.05). SGA infants had a
higher gestational age than AGA GR infants (31.1 (1.6) versus
30.1 (2.0) weeks, P o0.05). AGA GR+ and SGA infants had lower
weight and length SDS at term age and at 6 months post-term, as
well as higher weight and length SDS between term age and
6 months post-term compared with AGA GR infants (Table 1).
When fed formula, AGA GR+ and SGA infants had a higher protein,
energy and fat intake compared with AGA GR infants between
term age and 6 months post-term (Table 2). At term age, AGA GR+
and SGA infants had lower LM, FM and %FM compared with AGA
GR infants (Table 1). At 6 months post-term, AGA GR+ and SGA
infants had similar LM and lower FM and %FM compared with
AGA GR infants (Table 1). Between term age and 6 months postterm, AGA GR+ and SGA infants had higher LM and lower FM
compared with AGA GR infants (Table 1).
DISCUSSION
The present study suggests that, compared with AGA
GR infants, higher weight gain in AGA GR+ and SGA infants
consists of higher LM accretion and lower FM accretion during the
rst 6 months post-term. It has been demonstrated that FM
accumulation of preterm infants is positively related to energy and
protein intake after term age,8 as well as to weight gain during

Department of Pediatrics, VU University Medical Center, Amsterdam, The Netherlands. Correspondence: Dr M van de Lagemaat, VU University Medical Center, PO Box 7057,
1007 MB Amsterdam, The Netherlands.
E-mail: m.vandelagemaat@vumc.nl
Received 13 November 2013; revised 12 July 2014; accepted 29 July 2014; published online 17 September 2014

Fat mass and growth in preterm infants

M van de Lagemaat et al

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Table 1.

Growth and body composition in AGA GR , AGA GR+ and SGA infants
AGA GR (n = 83)

Birth
Weight
g
SDS
Length
cm
SDS
Term age
Weight
g
SDS
Length
cm
SDS
LM
g
FM
g
%FM
%
6 Months post-term
Weight
g
SDS
Length
cm
SDS
LM
g
FM
g
%FM
%

AGA GR+ (n = 15)

SGA (n = 33)

Absolute

Absolute

Absolute

83
83

1465 (371)a,b
0.12 0.67a,b

15
15

1182 (220)c
0.89 0.57c

33
33

1160 (468)
1.48 0.67

83
83

39.0 (3.5)a,b
0.27 0.84a,b

15
15

38.0 (2.0)c
0.86 0.73

33
33

36.0 (3.5)
2.51 0.46

83
83

3230 (465)a,b
0.45 0.8a,b

15
15

2641 (300)
2.25 0.48

33
33

2736 (574)
2.1 1.1

83
83

49.5 (2.0)a,b
0.55 0.85a,b

15
15

47.5 (3.0)c
1.78 0.98c

33
33

46.5 (3.5)
2.44 1.19

68

3112 (390)a,b

14

2652 (210)

28

2708 (430)

68

433 (240)a,b

14

146 (180)

28

142 (180)

68

a,b

14

5.1 (6.0)

28

4.9 (4.6)

11.8 (6.2)

83
83

7460 (1300)a,b
0.003 1.06a,b

15
15

6840 (1503)
0.91 1.01

33
33

6625 (1560)
1.13 1.12

83
83

67.0 (3.0)a,b
0.09 0.96a,b

15
15

66.0 (3.5)c
0.54 0.82c

33
33

64.0 (4.0)
1.16 1.1

66

5603 (730)

12

5442 (760)

24

5612 (890)

66

a,b

2082 (830)

12

1514 (660)

24

1628 (890)

66

25.5 (10.7)a,b

12

21.7 (9.4)

24

21.8 (7.7)

Abbreviations: AGA GR , appropriate-for-gestational-age without growth restriction at term age; AGA GR+, appropriate-for-gestational-age with growth
restriction at term age; FM, fat mass; LM, lean mass; SDS, standard deviation score; SGA, small-for-gestational-age. Values as median (interquartile range) or
median s.d. Differences compared by regression analyses adjusted for gender and gestational age. aAGA GR versus AGA GR+, P o0.05. bAGA GR versus
SGA, P o0.05. cAGA GR+ versus SGA, Po0.05.

Table 2.

Protein, energy, fat and carbohydrate intake between birth and 6 months post-term in formula-fed AGA GR , AGA GR+ and SGA infants
AGA GR

Term age6 months post-term

AGA GR+

SGA

Value

Value

Value

Protein intake
g/kg/day
g/day

52
52

2.38 0.25a,b
18.2 2.5

12
12

2.66 0.27
18.4 2.6

21
21

2.58 0.39
18.1 2.5

Energy intake
kcal/kg/day
kcal/day

52
52

12
12

109.6 10.0
758.2 101.1

21
21

106.9 13.5
753.1 83.9

Fat intake
g/kg/day
g/day

52
52

5.21 0.38a,b
39.7 4.8

12
12

5.65 0.54
39.1 5.0

21
21

5.56 0.68
39.2 4.7

Carbohydrate intake
g/kg/day
g/day

52
52

10.7 0.9a,b
81.4 10.7

12
12

11.8 1.2
81.7 11.8

21
21

11.5 1.6
80.7 8.9

99.8 7.5a,b
760.9 94.0

Abbreviations: AGA GR , appropriate-for-gestational-age without growth restriction at term age; AGA GR+, appropriate-for-gestational-age with growth
restriction at term age; SGA, small-for-gestational-age. Values as mean s.d. or median (interquartile range). Differences compared by regression analyses
adjusted for gender and gestational age. aAGA GR versus AGA GR+, P o0.05. bAGA GR versus SGA, Po 0.05.

European Journal of Clinical Nutrition (2014) 1261 1263

2014 Macmillan Publishers Limited

Fat mass and growth in preterm infants

M van de Lagemaat et al

early infancy.4 Therefore, it was remarkable in the present study

that FM at 6 months post-term was lower in AGA GR+ and SGA
preterm infants, whereas they had higher weight gain and
nutritional intakes compared with AGA GR infants during the
rst 6 months post-term. This is in contrast to a previous study
that shows that AGA GR+ infants are capable of recovering from
postnatal growth restriction during the rst 5 months post-term
with respect to their weight, length and %FM, whereas SGA
preterm infants reach a lower body weight with similar %FM.8
In the present study, lower dietary intake of nonprotein energy
after term age may delay FM restoration.9 With respect to FM
accretion, our ndings might support the premise5,10 that AGA GR
+ and SGA infants may benet from even higher nutritional
intakes than those achieved with the current feeding regimen
during infancy. On the other hand, not the absolute amount of
body fat but the delta body fat accumulation may have adverse
metabolic consequences in later life. In addition to nutritional
intake, body composition acquisition may depend on the genetic
growth potential. A genetically smaller body size of AGA GR+ and
SGA preterm infants may explain the lower FM accumulation
during the rst 6 months post-term. Another explanation for the
lack of FM restoration in AGA GR+ and SGA preterm infants may
be the timing of body composition measurement, as complete FM
restoration may occur later in life.
The present study had several limitations. The sample size was
relatively small, in particular after subgroup classication. This
study was part of a randomized trial on postdischarge nutrition
with a similar distribution of the type of diet between groups.
However, the inuence of the nutritional regimen cannot be
excluded completely. Another limitation was that the rst body
composition measurement occurred at term age and not a birth,
as a consequence of the original study design.
In conclusion, compared with AGA GR preterm infants, SGA
and AGA GR+ preterm infants restore their LM without excessive
FM accumulation at 6 months post-term despite a higher
nutritional intake (/kg/day) between term age and 6 months
post-term. It remains controversial whether higher nutritional
intakes that may potentially increase FM accretion are desirable in
AGA GR+ and SGA infants. Therefore, it is recommended to
carefully monitor early effects of nutritional intakes on body

2014 Macmillan Publishers Limited

1263
composition in preterm infants in order to prevent excessive FM
accretion that is associated with a higher risk of adiposity and
metabolic consequences in later life.
CONFLICT OF INTEREST
The authors declare no conict of interest.

ACKNOWLEDGEMENTS
This work was supported by an unrestricted research grant of FrieslandCampina,
Leeuwarden, The Netherlands.

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European Journal of Clinical Nutrition (2014) 1261 1263

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