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Clinical Experience in Enteral Nutrition Support for Premature
Infants With Bronchopulmonary Dysplasia
Maria A. Puangco, MS, RD, CNSD
Richard J. Schanler, MD, FAAP
OBJECTIVE:
The comprehensive management of infants with bronchopulmonary
dysplasia (BPD) may include the need for fluid restriction. Modular
nutrient components added to preterm formulas increase energy and
protein contents but may compromise the nutrient integrity of the formula. The purpose of this pilot study was to compare the nutritional
status and feeding tolerance of infants fed either a 30 kcal/oz ready-tofeed formula or a preterm formula containing nutrient supplements.
METHODS:
Feeding tolerance, growth, and biochemical indicators of nutritional
status were compared in 27 premature infants with BPD who were fluidrestricted. These infants were fed either a 30 kcal/oz ready-to-feed formula or a preterm formula with additives concentrated to 30 kcal/oz.
RESULTS:
Growth and feeding tolerance were similar between groups. Serum albumin and blood urea nitrogen concentrations, however, were improved in
the ready-to-feed formula group.
CONCLUSION:
A 30 kcal/oz ready-to-feed formula provides similar nutrient composition
but improved protein nutritional status; this formula is a safe alternative
to preterm formula containing multiple nutrient additives in premature
infants with BPD.
Journal of Perinatology 2000; 2:87–91.
The nutritional management of infants with bronchopulmonary
dysplasia (BPD) is a challenge for the clinician due to numerous
factors that affect the provision and utilization of nutrients. Factors
such as greater energy expenditure,1– 4 diuretic therapy,5,6 and fluid
restriction,7 become major problems because they compromise
growth, the optimal therapy for these infants.8,9
Twenty-four calorie per ounce preterm formulas originally were
designed to meet the needs of the growing healthy premature infant
when administered at a volume of ⬃150 ml/kg per day. When the
respiratory management of an infant with BPD requires fluid restriction, modular nutrient components added to preterm formulas improve energy and protein intake but may compromise the overall
nutrient integrity of the formula,10 increase its osmolality,10,11 and
dilute the mineral and micronutrient components of the formula.
The American Academy of Pediatrics recommends that formulas for
normal infants have concentrations of no greater than 450 mOsm/kg
H2O. 12 Several institutions also use routine powdered infant formula
or infant formula concentrate mixed with preterm formula to enhance nutrient intake. These enteral nutrient admixtures also may
adhere to the feeding tube and bottle, decrease milk flow through
small caliber feeding tubes, and diminish nutrient delivery to the
infant.10
To avoid the use of enteral admixtures, we evaluated a ready-tofeed formula in the management of older premature infants with
BPD. The purpose of this pilot study was to evaluate growth, feeding
tolerance, and the potential for nutrient inadequacies in premature
infants with BPD fed either a ready-to-feed formula or a preterm
formula containing a variety of nutrient supplements.
METHODS
Section of Neonatology (M. A. P., R. J. S.) and Children’s Nutrition Research Center (R. J. S.),
Department of Pediatrics, Baylor College of Medicine, Houston, TX.
R. J. S. is supported by the National Institute of Child Health and Human Development
(Grant RO-1-HD-28140) and by the General Clinical Research Center, Baylor College of
Medicine/Texas Children’s Hospital Clinical Research Center (Grant MO-1-RR-00188), National Institutes of Health. Partial funding was also provided by the U.S. Department of Agriculture (USDA)/Agricultural Research Service (ARS) under Cooperative Agreement No. 586250-6-001. This work is a publication of the USDA/ARS Children’s Nutrition Research
Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital
(Houston, TX). The contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations
imply endorsement by the U.S. Government.
Address correspondence and reprint requests to Richard J. Schanler, MD, Children’s Nutrition Research Center, 1100 Bates Street, Houston, TX 77030. E-mail address:
[email protected]
This review describes how two enteral formulas were used in our nurseries. Permission to review patient records was approved by the Institutional Review Board for Human Subject Research of Baylor College
of Medicine (Houston, TX). All subjects were newborn infants admitted to the neonatal intensive care unit at Texas Children’s Hospital
between 1994 and 1998. Infants with a diagnosis of BPD, a persistent
oxygen requirement beyond 28 days of age with compatible chest
radiographic changes,13 who were fed commercial formula and
treated with a fluid restriction of ⱕ130 ml/kg per day were followed
longitudinally throughout their hospital course by the Neonatal Nutrition Team. Initially, all infants were fed 24 kcal/oz preterm formula with iron (Enfamil Premature Formula; Mead Johnson Nutri-
Journal of Perinatology 2000; 2:87–91
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87
Puangco and Schanler
Nutritional Support for Premature Infants with BPD
Table 1 Nutrient Composition of Ready-To-Feed Formula and
Preterm Formula With Additives
Energy, kcal/dl
Protein, g/dl (% calories)
Fat, g/dl (% calories)
Carbohydrate, g/dl (% calories)
Calcium, mg/dl
Phosphorus, mg/dl
Chloride, mEq/dl
Vitamin A, IU#/dl
Vitamin E, IU/dl
Vitamin D, IU/dl
Group A
(ready-to-feed
formula)*
Group B
(preterm formula
with additives)‡
101
3.0 (12)
4.9 (44)
11.2 (44)
96
79
2.9
1754†
7.3†
450†
111
2.9 (10)§
6.1 (49)¶
11.2 (40)㛳
132
66
2.0
1000
5.1
216
*PediaSure (Ross Products Division, Abbott Laboratories), 1 ml per day.
†Poly-Vi-Sol (Mead Johnson Nutritionals), 1 ml per day.
‡Enfamil Premature Formula 24 with iron (Mead Johnson Nutritionals) with §protein
additive, Casec (Mead Johnson Nutritionals) at 0.5 g/dl formula, plus ¶corn oil additive,
2 ml/kg per day divided four times daily given separately, and 㛳carbohydrate additive,
Polycose (Ross Products Division, Abbott Laboratories) to 27 kcal/oz.
#International units.
tionals, Evansville, IN) at 150 ml/kg per day. When fluid restriction
was initiated, infants were given the preterm formula plus glucose
polymers (Polycose; Ross Products Division, Abbott Laboratories,
Columbus, OH) usually prepared to 27 kcal/oz and individual doses of
corn oil (⬃2 ml/kg per day) calculated to provide a milk concentration of ⱖ30 kcal/oz (Table 1). Ultimately, at the discretion of the
attending neonatologist, a subgroup of these infants was given a
ready-to-feed 30 kcal/oz formula (PediaSure; Ross Products Division,
Abbott Laboratories). The ready-to-feed formula was used after the
infant had attained a chronological age of 4 months or at ⱖ44 weeks
postmenstrual age. The transition to the ready-to-feed formula was
made by increasing the feedings by one feed per day as tolerated by
the infant. The remaining infants were maintained on the preterm
formula with additives.
The two groups (group A, infants that eventually received the
ready-to-feed formula; group B, infants that continued to receive the
preterm formula with additives) were evaluated during three phases.
In phase 1 (A1, B1), infants received 24 kcal/oz preterm formula with
iron at 150 ml/kg per day. In phase 2 (A2, B2), all infants’ fluids were
restricted to ⱕ130 ml/kg per day using preterm formula with additives. In phase 3 (A3, B3), the infants received further fluid restriction
provided as either the ready-to-feed formula (A3) or preterm formula
with additives (B3).
Growth was evaluated weekly. Weight was measured daily to the
nearest 1 gm using electronic scales (Model 4800, Scale Tronix,
Wheaton, IL). Recumbent length, to the nearest 0.1 cm (O’Leary
Newborn Length Board; Ellard Instrumentation, Seattle, WA) was
measured at 36 weeks’ postmenstrual age and monthly thereafter.
Biochemical indicators of nutritional status, albumin, alkaline phos88
Table 2 Characteristics of Infants Evaluated
Group A (ready-to- Group B (preterm
feed formula)
formula with
(n ⫽ 16)
additives)
(n ⫽ 11)
Birth weight (gm)
1200* (733, 2540) 694 (640, 1074)
Gestation (weeks)
30 (25, 33)
25 (24, 27)
Gender (males⬊females)
7⬊9
8⬊3
Duration of mechanical ventilation 168 (78, 270)
103 (68, 113)
(days)
Postnatal steroid therapy (days)
9 (0, 37)
11 (8, 16)
Diuretic therapy (days)
126 (71, 173)
87 (70, 106)
Antibiotic therapy (days)
44 (35, 61)
38 (18, 49)
Postmenstrual age fluid restricted to 44† (40, 52)
36 (32, 40)
ⱕ130 ml/kg per day (weeks)
Postnatal age when fluid restriction 110‡ (80, 131)
63 (45, 94)
imposed (days)
Body weight when fluid restriction 3198‡ (1966, 4300) 1685 (833, 2855)
imposed (gm)
Duration of hospitalization (days) 256‡ (179, 323)
178 (159, 194)
ⴱMedian (25th, 75th percentiles).
†P ⬍ 0.005.
‡ P ⬍ 0.05.
phatase activity, phosphorus, and blood urea nitrogen (BUN) were
measured every other week throughout hospitalization. Fluid intake
(type and amount), urine output, and indices of feeding tolerance
were assessed daily. Overall fluid balance was assessed by daily intake
and output, body weight changes, and the measurement of serum
electrolytes twice weekly. Nutrient intake was analyzed for potential
deficiencies using Neonova (Ross Products Division, Abbott Laboratories), a neonatal nutrition software program. Feeding tolerance was
determined by a change in stool pattern, abdominal distention, a
change in gastric residual volume, and/or emesis. The duration of
therapy with diuretic, glucocorticoid, and antibiotic medications as
well as number of infants receiving anti-gastroesophageal reflux
medications were tabulated.
Statistical comparisons of clinical characteristics between groups
were made using nonparametric methods. Statistical comparisons of
intakes, growth, feeding tolerance, and biochemical indicators of
nutritional status were made using repeated measures analysis of
variance. Results demonstrating probability levels of ⱕ0.05 were
considered significant. Unless indicated otherwise, the data were expressed as median and 25th and 75th percentiles.
RESULTS
A total of 27 infants with BPD requiring severe fluid restriction between November of 1994 and December of 1998 participated in this
evaluation. In phase 3, 16 infants were switched from preterm formula to the ready-to-feed formula (A3) and 11 infants continued to
receive a preterm formula plus additives (B3). The clinical characterJournal of Perinatology 2000; 2:87–91
Nutritional Support for Premature Infants with BPD
Puangco and Schanler
Table 3 Actual Fluid and Nutrient Intakes in Groups A and B During Phases 1, 2, and 3
Component
Group
Phase 1*
Phase 2†
Phase 3‡
Fluid§ (ml/kg per day)
A
B
143 ⫾ 21
150 ⫾ 12
132 ⫾ 15
131 ⫾ 17
116 ⫾ 14
125 ⫾ 14
Calorie (kcal/kg per day)
A
B
121 ⫾ 19
127 ⫾ 13
119 ⫾ 20
126 ⫾ 11
112 ⫾ 17
122 ⫾ 15
Protein (g/kg per day)
A
B
3.0 ⫾ 0.6
3.1 ⫾ 0.4
2.9 ⫾ 0.5
3.0 ⫾ 0.5
3.3 ⫾ 0.4
3.2 ⫾ 0.6
Additional protein¶ (g/kg per day)
A
B
0.02 ⫾ 0.08
0.04 ⫾ 0.15
0.25 ⫾ 0.56
0.43 ⫾ 0.55
0
0.47 ⫾ 0.50
Additional carbohydrate and/or fat (kcal/kg per day)
A
B
5⫾8
9 ⫾ 13
13 ⫾ 13
15 ⫾ 13
6 ⫾ 11
18 ⫾ 11
Chloride supplement (mEq/kg per day)
A
B
4⫾3
3⫾4
4⫾3
5⫾4
2⫾2
3⫾3
*All infants received preterm formula with iron at 150 ml/kg per day. Group A received ready-to-feed formula and group B received preterm formula with additives.
†All infants received preterm formula with additives at 130 ml/kg per day. Group A received ready-to-feed formula and group B received preterm formula with additives.
‡Further fluid restriction was imposed. Group A received ready-to-feed formula and group B received preterm formula with additives. Group designation was based on diet in phase 3.
§Significant differences over time (phase 1 to phase 3), p ⫽ 0.001; differences between groups were not significant.
¶Significant differences over time (phase 1 to phase 3), p ⬍ 0.005; interaction between groups, p ⫽ 0.002. Significant difference between groups in phase 3, p ⫽ 0.01.
istics of the 27 infants are shown in Table 2. Group A was older and
attained a greater body weight than group B when fluid restriction
was initiated in phase 2. The duration of hospitalization also was
longer for the infants in group A. The nutrition parameters for each
treatment group and phase are shown in Tables 3 and 4. There were
no differences in fluid and milk intake between groups. However, milk
intake decreased in both groups over time (Table 3). Calorie, protein,
and modular calorie intake were similar between groups. Modular
protein intake increased over time for the infants in group C. Chloride
supplementation was similar between groups. The tabulation of nutrient intakes indicated that group A, during phase A3, had marginal
vitamin D intake. That group was given 1 ml per day of a multivitamin supplement (Poly-Vi-Sol, Ross Products Division, Abbott Laboratories). The number of infants requiring anti-gastroesophageal reflux
medications did not differ between groups, but increased over time
( p ⬍ 0.05). Weight velocity was similar between groups, but increased over time. Linear growth was similar between groups and over
time (Table 4). There were no differences in feeding tolerance between groups during any of the phases. The number of stools, however, was significantly more in group A compared with group B.
Biochemical indicators of protein nutritional status were improved in group A compared with group B (Table 4). There was a
significant group-time interaction for BUN concentration. BUN was
significantly greater in group A compared with group B during phase
3. Both serum phosphorus and alkaline phosphatase were similar
between groups and over time.
Journal of Perinatology 2000; 2:87–91
DISCUSSION
Infants with BPD require greater energy and protein intakes14 from
balanced nutrition sources, while avoiding excessive mineral intake to
decrease the risk of nephrocalcinosis.15 The therapy for infants with
BPD (steroids,2,4 diuretics,5,6 and fluid restriction7) also may compromise nutrition status. DeRegnier et al.16 demonstrated that low protein and calorie diets in infants with BPD were associated with less
arm fat and muscle accretion and slower growth at as early as 2 weeks
of age when compared with premature infants that never developed
BPD. In addition, when full enteral feeding was achieved, BPD infants
had growth velocities that were similar to those of controls; however,
these infants did not demonstrate catch-up growth.16 Growth failure
as a result of medical therapies, particularly fluid restriction, should
not be an assumed outcome. The use of preterm formula with additives is a common therapy practiced out of necessity in many neonatal
intensive care units for infants requiring fluid restriction. The benefit
of using nutrient additives is to maintain uniform nutrient intakes to
insure adequate growth in the chronically ill infant with BPD. One
disadvantage of using only calorie additives (such as glucose polymers or fat), however, is that they may dilute the protein, mineral,
and micronutrient content of the milk. In addition, nonprotein calorie additives may support weight gain due to fat accretion, but may
not increase lean body mass proportionately.17 The net effect of nutrient additives on absorption and/or the bioavailability of milk components has not been investigated. Several studies have shown that mix89
Puangco and Schanler
Nutritional Support for Premature Infants with BPD
Table 4 Growth, Feeding Tolerance, and Biochemical Indicators of
Nutritional Status
Measure
Group Phase 1*
20 ⫾ 7
14 ⫾ 8
Phase 2†
Phase 3‡
19 ⫾ 9
19 ⫾ 7
27 ⫾ 9
24 ⫾ 7
0.6 ⫾ 0.1
0.9 ⫾ 0
0.6 ⫾ 0.2
0.8 ⫾ 2
Weight gain§ (gm/day)
A
B
Length increment (cm/week)
A
B
Gastric residual volume (ml/day)
A
B
7 ⫾ 10
7⫾8
11 ⫾ 8
12 ⫾ 12
6⫾7
9 ⫾ 11
Emesis (ml/day)
A
B
3⫾6
2⫾5
6 ⫾ 10
5 ⫾ 11
6 ⫾ 10
5⫾4
Stool number¶ (#/day)
A
B
3⫾2
3⫾1
3⫾1
3⫾1
4⫾1
2 ⫾ 0.5
Albumin㛳 (mg/dl)
A
B
3.1 ⫾ 0.4 3.5 ⫾ 0.4
2.9 ⫾ 0.4 3.0 ⫾ 0.3
3.5 ⫾ 0.4
3.4 ⫾ 0.3
BUN# (mg/dl)
A
B
17 ⫾ 9
18 ⫾ 10
16 ⫾ 9**
11 ⫾ 5**
Serum phosphorus (mg/dl)
A
B
6.0 ⫾ 1 5.9 ⫾ 0.6
6.9 ⫾ 1.3 5.7 ⫾ 0.7
Alkaline phosphatase (IU††/liter)
A
B
307 ⫾ 136 296 ⫾ 108 300 ⫾ 96
322 ⫾ 168 282 ⫾ 101 272 ⫾ 98
13 ⫾ 7
9⫾5
6.0 ⫾ 0.7
6.2 ⫾ 0.7
*All infants received preterm formula with iron at 150 ml/kg per day. Group A received
ready-to-feed formula and Group B received preterm formula with additives.
†All infants received preterm formula with additives at 130 ml/kg per day. Group A received
ready-to-feed formula and Group B received preterm formula with additives.
‡Further fluid restriction was imposed. Group A received ready-to-feed formula and
Group B received preterm formula with additives. Group designation was based on diet in
phase 3.
§Significant differences over time (phase 1 to phase 3), p ⬍ 0.001; differences
between groups not significant.
¶Significant differences between groups, p ⬍ 0.01.
㛳Significant differences over time (phase 1 to phase 3), p ⬍ 0.001; significant
differences between groups, p ⬍ 0.01.
#Significant interaction between group and time, p ⬍ 0.01.
**Significant difference between groups during phase 3, p ⬍ 0.05.
††International units.
ing fat with formula results in fat separation and adherence to feeding
tubes.18,19 Saigal and Sinclair,20 compared feeding a 20 kcal/oz formula with feeding a 30 kcal/oz formula to low birth weight infants.
The only moderately adverse affect noted in that study was a higher
urine osmolality in infants that were fed the 30 kcal/oz formula compared with those infants that were fed the 20 kcal/oz formula.
In contrast, we report the use of a ready-to-feed 30 kcal/oz formula that is well tolerated in older premature infants with BPD. We
show that along with severe fluid restriction, less protein supplemen90
tation was needed over time in group A, and that the isosmolar readyto-feed formula supported the nutritional needs for this high-risk
population.21–23
Except for stool output, which differed but was not excessive,
feeding tolerance was similar between groups. One infant developed
watery stool output after the ready-to-feed formula was initiated. This
was attributed to the inadvertent use of ready-to-feed formula containing fiber and to a rapid transition to all ready-to-feed formula.
Weight velocity between groups was similar, but there was a significant time effect. In both groups, weight patterns improved over
time. This may be due to the decreasing energy needs of infants as
they mature. Serum albumin concentrations were significantly higher
in group A versus group B, owing to the higher protein content of the
ready-to-feed formula. Serum albumin also improved over time, and
this improvement may be associated with increased hepatic synthesis
of albumin as an infant matures. Although BUN was higher in group
A, it was within the accepted normal range; we speculate that this
signifies an improved protein nutritional status.24
The use of anti-reflux medications increased over time, but was
not significantly different between groups. This finding concurs with a
study by Radford et al.25 that indicated that gastroesophageal reflux is
more common in infants with BPD. An advantage of using a 30
kcal/oz formulation also may be the provision of a lower volume of
milk while continuing to meet nutrient needs.
Fewtrell et al.7 compared feeding a 30 kcal/oz formula (intake
145 ml and 145 kcal/kg per day) with feeding a preterm formula
(intake 180 ml and 150 kcal/kg per day) in premature infants of
ⱕ32 weeks’ gestational age and ⱕ1500 gm. They hypothesized that
the infants fed the 30 kcal/oz formula would have better growth than
those fed the preterm formula. Although the group receiving the 30
kcal/oz formula was less healthy, feeding tolerance was similar; however, the 30 kcal/oz group required a shorter duration of diuretic
therapy when compared with infants fed the 24 kcal/oz formula.
Importantly, the investigation reported no differences between groups
with regard to growth measures. Our results did not show a difference
in the duration of diuretic therapy between groups because our infants were older and were hospitalized for a longer duration.
Other institutions use routine term formula to concentrate nutrients in preterm formula when fluid restriction is necessary. Reimers et
al.14 described the use of a combination of preterm and term formula
in a ratio of 3:1. The osmolality was 388 mOsm/kg H2O compared
with the lower osmolality (300 mOsm/kg H2O) of the read-to-feed
formula used in our study. A comparison of the nutrient composition
of the two formulations shows that the ready-to-feed formula we used
had a higher protein and chloride content and more balanced nonprotein calories, which would be more favorable for the infant with
BPD. Jew et al.26 studied the osmolalities of the oral medications and
formulas used in their nursery. Although no osmolalities for 30
kcal/oz formulas were reported in their study, the osmolalities for
Pregestimil (Mead Johnson Nutritionals) and Enfamil Premature 24
mixed with Similac PM 60/40 (Ross Products Division, Abbott Laboratories) concentrated to 27 kcal/oz were 496 and 360 mOsm/kg H2O,
Journal of Perinatology 2000; 2:87–91
Nutritional Support for Premature Infants with BPD
respectively. At these concentrations, the nutrient content is similar to
the ready-to-feed formula we used, but the osmolalities are significantly greater.
We demonstrated that a ready-to-feed formula provides a similar
nutrient composition and nutritional status to preterm formula enhanced with multiple additives in premature infants with BPD. These
results also show that ready-to-feed formula is a safe alternative compared with providing a concentrated term formula to infants with
BPD requiring severe fluid restriction. Further study of the absorption
and bioavailability of supplements added to formulas as well as their
effects on body composition is warranted. We believe that the use of
ready-to-feed formula in larger and older premature infants should be
encouraged, because currently it is not approved for use in this population. There are other alternatives for providing nutrition to fluidrestricted infants. We recommend randomized clinical trials of readyto-feed 30 kcal/oz formulas and routine formula concentrated to 30
kcal/oz. These pilot data, however, indicate acceptance of the 30
kcal/oz ready-to-feed formula for the long-term management of
premature infants with BPD who require severe fluid restriction.
Acknowledgments
We thank Idelle Tapper for secretarial assistance.
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