Energy Expenditure for Breastfeeding and Bottle-Feeding Preterm Infants

  

Energy Expenditure for Breastfeeding and Bottle-Feeding Preterm Infants

Irit Berger, Valentin Weintraub, Shaul Dollberg, Rozalia Kopolovitz and Dror Mandel

  Pediatrics 2009;124;e1149-e1152; originally published online Nov 23, 2009;

DOI: 10.1542/peds.2009-0165

  

The online version of this article, along with updated information and services, is

located on the World Wide Web at:

  PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2009 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275. Energy Expenditure for Breastfeeding and Bottle-Feeding Preterm Infants WHAT’S KNOWN ON THIS SUBJECT:

  Most VLBW infants cannot be fed at the breast at birth, and feeding with expressed breast milk through a gastric tube is recommended. Sucking skills mature at ⬃34 weeks, when nipple-feeding is introduced.

  REE measurements for preterm infants immediately after feeding at the breast and after feeding of expressed breast milk by bottle are very similar.

  abstract OBJECTIVE:

  We hypothesized that resting energy expenditure (REE) would be higher after breastfeeding than after bottle-feeding.

  METHODS:

  Nineteen preterm infants (gestational age: 32 weeks) in stable condition who were nourished entirely with their mothers’ breast milk were assigned randomly to feeding either by bottle or at the breast. Each infant served as his or her own control subject. REE was measured for 20 minutes after feeding. Breast milk quantity was evaluated with prefeeding and postfeeding weighing. REE values for bottle-feeding and breastfeeding were compared with paired t tests.

  RESULTS:

  Contrary to our null hypothesis, the group’s mean REE val- ues after bottle-feeding and breastfeeding were very similar (284.7 ⫾ 26.8 kJ/kg per day [68.3 ⫾ 6.4 kcal/kg per day] vs 282.6 ⫾ 28.5 kJ/kg per day [67.5 ⫾ 6.8 kcal/kg per day]; not significant). The duration of feeding was significantly longer for breastfeeding than for bottle- feeding (20.1 ⫾ 7.9 vs 7.8 ⫾ 2.9 minutes; P ⬍ .0001). Maternal breast milk, with its well- documented nutritional and immuno- logic advantages for general health, growth, and development and possibly the enhancement of cognitive develop- ment, is the optimal method of infant feeding.

  

CONCLUSION:

  There was no significant difference in REE when infants were breastfed versus bottle-fed. Longer feeding times at the breast did not increase REE. We speculate that it is safe to recommend feeding at the breast for infants born at ⬎32 weeks when they can tolerate oral feeding. Pediatrics 2009;124:e1149–e1152

  AUTHORS: Irit Berger, MD, Valentin Weintraub, PhD, Shaul Dollberg, MD, Rozalia Kopolovitz, RN, and Dror Mandel, MD Department of Neonatology, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

KEY WORDS

  metabolic rate, indirect calorimetry, oral feeding ABBREVIATIONS REE—resting energy expenditure

  VLBW—very low birth weight This trial has been registered at www.clinicaltrials.gov (identifier NCT00838188). www.pediatrics.org/cgi/doi/10.1542/peds.2009-0165 doi:10.1542/peds.2009-0165 Accepted for publication Jun 23, 2009 Address correspondence to Shaul Dollberg, MD, Department of Neonatology, Tel Aviv Sourasky Medical Center, 6 Weizman St, Tel Aviv 64239, Israel. E-mail: dolberg@post.tau.ac.il PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2009 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

  ARTICLES

WHAT THIS STUDY ADDS:

  1–4

  Study Design

  RESULTS We recruited 20 infants for the study.

  We used computer-generated random numbers in sealed opaque envelopes to assign the breast/bottle sequence. Statistical analysis of REE values with breastfeeding and bottle-feeding was performed with the paired t test and regression analysis. Results are ex- pressed as mean ⫾ SD. P values of .05 were considered significant.

  28,29 Statistical Analysis

  traassay coefficient of variation of 3% in our hands, and it has been used ex- tensively for small infants by other investigators.

  27 The instrument has an in-

  ies have shown the technique to give results equivalent to direct measure- ments.

  26 Validation stud-

  values are determined with the Fick principle, in which gas production or consumption ⫽ (concentration differ- ence in inspired and expired gas) ⫻ total gas flow. This method is safe and allows prolonged measurements while allowing reasonable access to the in- fant for routine care.

  25 The

  Metabolic measurements were per- formed through indirect calorimetry. They were conducted while the infants were prone and asleep, by using a Del- tatrac II metabolic monitor (Datex- Ohmeda, Helsinki, Finland). The instru- ment uses the principle of an open circuit system that allows continuous measurements of oxygen consumption and carbon dioxide production.

  23,24 Measurements

  This was a prospective, randomized in- vestigation. Each infant was evaluated twice on a single day at 2 consecutive meals, once after breastfeeding and once after bottle-feeding of breast milk by using a premature nipple and ring (Ross Products Division, Columbus OH). In this way, each infant served as his or her own control subject. REE was re- corded for 20 minutes after each meal. The duration of each meal and the creamatocrit of the bottle, and at the beginning and the end of every feeding at the breast were measured as de- scribed previously.

  Our institutional review board and the national Ministry of Health approved this study, and signed informed con- sent was obtained from both parents of each infant. Preterm infants who were born at ⱖ32 weeks of gestation and had reached the corrected gesta- tional age of ⱖ34 weeks were in- cluded. Infants in thermally stable con- dition were cared for in open unwarmed bassinets and were held by their moth- ers during feeding. The infants were all fed solely with their mothers’ breast milk starting during the first week of life, equivalent to ⱖ150 mL/kg per day divided into 8 meals, and were growing steadily. They were considered ready to be recruited into the study when they could feed ⱖ1 full meal at the breast. Estimation of the amount of milk ingested was performed by test- weighing or by measuring the volume received by bottle. Infants who fed ⬍25 mL from either bottle or breast, in- fants who required supplemental ox- ygen for ⱖ1 week before recruit- ment, infants diagnosed as having active infections, and infants with a patent ductus arteriosus were ex- cluded. We also excluded infants with congenital anomalies and infants who had either ⬎5 daily episodes of apnea of prematurity or any apnea requiring assistance or methylxan- thine therapy.

  Human milk conveys spe- cific advantages in improved host de- fense,

  METHODS Study Population

  The primary goal of this study was to compare resting energy expenditure (REE) for preterm infants fed their moth- ers’ expressed milk by bottle or fed at the breast. We hypothesized that the REE would be higher with breastfeeding than with bottle-feeding.

  19–22

  In the absence of evidence-based data to determine the best time to introduce breastfeeding, many clinicians use empiric criteria, such as the infant’s weight, gestational age, and ability to bottle-feed, as prox- ies of readiness to breastfeed. Despite some evidence of physiologic benefits of preterm infants feeding at the breast, many neonatologists consider direct breastfeeding to be too fatiguing for preterm infants. It is not known, how- ever, whether preterm infants who are breastfed expend more energy than bottle-fed infants.

  15–18

  Most VLBW infants cannot be fed at the breast at birth, and feeding with expressed breast milk through a gas- tric tube is recommended. Sucking skills mature at ⬃34 weeks, when nipple- feeding is introduced.

  12–14

  and there are even a number of studies that indicate potential health benefits for breastfeeding mothers.

  10,11

  for very low birth weight (VLBW) infants. Psychological and developmen- tal benefits also have been reported,

  8,9

  suitability for gut absorption, more-rapid gastric emptying, and re- duced risk of necrotizing enterocoli- tis

  5–7

  One infant was excluded after random- ization because he breastfed only 5 mL. There were 12 boys and 7 girls. The mean birth weight was 1859 ⫾ 227 g (range: 1480 –2210 g), and the mean weight at the time of the study was 2147 ⫾ 188 g. The mean gestational age was 33 ⫾ 1.4 weeks, and the chro- nologic age at the time of the study was 22 ⫾ 9 days. The creamatocrit mea- surement in the milk given by bottle (6.7 ⫾ 1.4%) was similar to the averaged creamatocrit values of the initial and fi- nal breast milk samples (6.1 ⫾ 1.4%; P ⫽ .09). Infants spent significantly more time at the breast (20.1 ⫾ 7.9 minutes) than when fed by bottle (7.8 ⫾ 2.9 min- utes; P ⬍ .0001). There were no signifi- cant differences in the volume of milk consumed through breastfeeding ver- sus bottle-feeding (42 ⫾ 11.1 vs 43.56 ⫾ 5.0 mL; P ⫽ .62) or in REE per volume of milk intake (6.8 ⫾ 2.4 vs 0.5 ⫾ 5.7 kJ/kg/ ml/d; P ⫽ .23). Contrary to our null hy- pothesis, there was no significant differ- ence in REE after direct breastfeeding versus bottle-feeding (284.7 ⫾ 26.8 kJ/kg per day [68.3 ⫾ 6.4 kcal/kg per day] vs 282.6 ⫾ 28.5 kJ/kg per day [67.5 ⫾ 6.8 kcal/kg per day]; P ⫽ .7) (Table 1). Moreover, we could not find any consis- tent trends, because 5 infants had higher REE values after breastfeeding than after bottle-feeding, whereas the others showed a reverse pattern. The re- sults of regression analysis with the difference in REE with bottle-feeding ver- sus breastfeeding as the dependent vari- able and the duration of feeding as the independent variable were not signifi- cant (P ⫽ .8). We also found no correla- tions between the difference in REE with breastfeeding versus bottle-feeding and gestational age, chronologic age, birth weight, or weight at the time of exami- nation. The difference in the volume of milk ingested through breastfeeding versus bottle-feeding did not exceed 5 mL for any of the infants.

  In addition, we demonstrated very simi- lar REE values immediately after feeding for our 20 preterm study infants fed breast milk directly at the breast or ex- pressed into a bottle, and longer feeding time at the breast did not increase REE. We would have needed ⬃1300 infants to detect a significant difference if one ex- isted (P ⫽ .05; power ⫽ 0.8).

  33 We studied preterm infants who were

  .48 Oxygen consumption, mean ⫾ SD, mL/kg per min 21 ⫾ 1.5 21 ⫾ 1.9 .84

  .62 REE, mean ⫾ SD, kJ/kg per d 284.7 ⫾ 26.8 282.6 ⫾ 28.5 .7 Respiratory quotient, mean ⫾ SD 0.85 ⫾ 0.04 0.85 ⫾ 0.03 .5 Carbon dioxide production, mean ⫾ SD, mL/kg per min 18 ⫾ 1.3 18 ⫾ 1.5

  Crematocrit level, mean ⫾ SD, % 6.1 ⫾ 1.4 6.7 ⫾ 1.4 .09 Duration of feeding, mean ⫾ SD, min 20.1 ⫾ 7.9 7.8 ⫾ 2.9 ⬍.001 Volume of intake, mean ⫾ SD, mL 42.2 ⫾ 11.1 43.5 ⫾ 5.0

  TABLE 1 REE and Clinical and Laboratory Outcomes for Infants Who Were Breastfed or Bottle-Fed Their Mother’s Milk Variable Breastfeeding Bottle-Feeding P

  in the current study immediately after feeding because we expected that the

  29 We measured the REE

  One potential limitation of our study is the timing of the measurement of REE. We studied infants immediately after feeding, because measurements during breastfeeding were not technically pos- sible. From our previous study, we knew that the REE increases from baseline to the time of gavage feeding and further increases during the immediate post- prandial period.

  and the longer duration of feeding at the breast led us to hypothesize that REE values also would be different. De- spite these other distinct differences, we found that REE values were very similar with the 2 methods of feeding.

  34

  strongly supports the use of breast milk rather than preterm formula, from an energy balance point of view. Whether there is any difference in REE between feeding of breast milk directly at the breast or by bottle has not been studied before. The fact that the me- chanics of sucking and swallowing at the breast are significantly different from those with artificial nipples, as demonstrated with ultrasonography,

  29 This finding

  gavage-fed their own mother’s milk or preterm infant formula, and we found significantly lower REE values during breast milk feeding.

  but also for preterm infants.

  DISCUSSION

  32

  would potentially extend the duration of breastfeeding for these mothers. Another potential concern may be nip- ple confusion, which has been re- ported mostly for term infants

  31 Earlier feeding at the breast

  showed that small preterm infants at corrected gestational age of 35 weeks had improved physio- logic responses with breastfeeding than with bottle-feeding, in terms of higher oxygen saturation, higher body tem- perature, and fewer desaturation events. It is also widely accepted that mothers of preterm infants stop lacta- tion earlier than do mothers of term infants.

  20

  and may afford, among other factors, the ability to measure the exact volume of each meal, the ability to feed infants without transferring them from the in- cubator, and the ability to put into practice the notion that nurses with expertise may achieve better success in reaching full oral feeding faster. A study by Meier

  30

  Introduction of bottle-feeding before breastfeeding had been com- mon practice among neonatologists

  19–21

  At that time, the introduction of oral feedings depends on a learning process on the part of the preterm infant. Introduction of small quantities and increases to full oral feedings may take days or even weeks. The optimal timing of the first breastfeeding opportunity for preterm infants has not been studied systemat- ically. Clinicians have used empiric criteria, such as infant weight, gesta- tional age, and ability to bottle-feed, as indicators of readiness to breast- feed.

  

15–19

  Preterm infants lack the physiologic maturity for effective suck-swallow un- til they reach the corrected gestational age of ⬃34 weeks.

  ARTICLES infants who expended more energy during breastfeeding would have higher REE values in the immediate postprandial period. Our study in- cluded periods of nonnutritive sucking for both modes of feeding. We do not know the relative contributions of nu- tritive and nonnutritive sucking to REE.

  CONCLUSIONS

  26. Bauer K, Pasel K, Uhrig C, Sperling P, Ver- smold H. Comparison of face mask, head hood, and canopy for breath sampling of flow through indirect calorimetry to mea- sure oxygen consumption and carbon monoxide production of preterm infants less than 1500 grams. Pediatr Res. 1997; 41(1):139 –144

  

18. Lau C, Smith EO, Schanler RJ. Coordination

of suck-swallow and swallow-respiration in preterm infants. Acta Paediatr. 2003;92(6): 721–727

  

19. Meier P, Anderson GC. Responses of small

preterm infants to bottle- and breast- feeding. MCN Am J Matern Child Nurs. 1987; 12:97–105

  

20. Meier P. Bottle- and breastfeeding: effects

of transcutaneous oxygen pressure and temperature in preterm infants. Nurs Res. 1988;37(1):36 – 41

  

21. Chen CH, Wang TM, Chang HM, Chi CS. The

effect of breast- and bottle-feeding on oxy- gen saturation and body temperature in preterm infants. J Hum Lact. 2000;16(1): 21–27

22. Bier JB, Ferguson A, Anderson L, et al.

Breast-feeding of very low birth weight in-

fants. J Pediatr. 1993;123(5):773–778

  Creamatocrit: simple clinical technique for estimating fat concentration and energy value of human milk. Br Med J. 1978; 1(6119):1018 –1020

  

24. Meier PP, Engstrom JL, Murtaugh MA, Vasan

U, Meier WA, Schanler RJ. Mothers’ milk feedings in the neonatal intensive care unit: accuracy of the creamatocrit technique.

  J Perinatol. 2002;22(8):646 – 649 25. Je´quier E, Felber J. Indirect calorimetry. Ballieres Clin Endocrinol Metab. 1987;1(4): 911–935

  27. Olhager E, Forsum E. Total energy expendi- ture, body composition and weight gain in moderately preterm and full-term infants at term postconceptional age. Acta Paediatr. 2003;92(11):1327–1334

  

Dev Med Child Neurol. 2001;43(1):22–27

  28. Lubetzky R, Vaisman N, Mimouni FB, Doll- berg S. Energy expenditure in human milk- versus formula-fed preterm infants. J Pedi- atr. 2003;143(6):750 –753 29. Bauer K, Laurenz M, Ketteler J, Versmold H.

  Longitudinal study of energy expenditure in preterm neonates ⬍30 weeks’ gestation during the first three postnatal weeks. J Pe- diatr. 2003;142(4):390 –396

  30. Sheppard JJ, Fletcher KR. Evidence-based interventions for breast and bottle feeding in the neonatal intensive care unit. Semin Speech Lang. 2007;28(3):204 –212

  31. Lefebvre F, Ducharme M. Incidence and du- ration of lactation and lactational perfor- mance among mothers of low-birth-weight and term infants. CMAJ. 1989;140(10): 1159 –1164

  32. Neifert M, Lawrence R, Seacat J. Nipple confusion: toward a formal definition. J Pe- diatr. 1995;126(6):S125–S129

  33. Nye C. Transitioning premature infants from gavage to breast. Neonatal Netw. 2008; 27(1):7–13

  34. Nowak AJ, Smith WL, Erenberg A. Imaging evaluation of breast-feeding and bottle- feeding systems. J Pediatr. 1995;126(6): S130 –S134

  

17. Mizuno K, Ueka A. The maturation and coor-

dination of sucking, swallowing, and respi- ration in preterm infants. J Pediatr. 2003; 142(1):36 – 40

  

16. Gewolb IH, Schwietzer-Kenney EL, Taciak VL,

Bosma JF. Developmental patterns of rhyth- mic suck and swallow in preterm infants.

  We conclude that REE measurements for preterm infants immediately af- ter feeding at the breast and after feeding of expressed breast milk by bottle are very similar. We speculate that allowing infants to feed at the breast as soon as they can tolerate feedings by mouth would not jeopar- dize energy balance and has mani- fold nutritional, physiologic, and emotional benefits.

  5. Howie PW, Forsyth JS, Ogston SA, Clark A, Florey CD. Protective effect of breast feed- ing against infection. BMJ. 1990;300(6716): 11–16

  ACKNOWLEDGMENT

  Esther Eshkol is thanked for her edito- rial assistance.

  REFERENCES

  1. American Academy of Pediatrics, Work Group on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics. 1997; 100(6):1035–1039

  2. Schanler RJ. Evaluation of the evidence to support current recommendations to meet the needs of premature infants: the role of human milk. Am J Clin Nutr. 2007;85(2): 625S– 628S

  3. Schanler RJ. The use of human milk for pre- mature infants. Pediatr Clin North Am. 2001; 48(1):207–219

  4. Schanler RJ, Shulman RJ, Lau C. Feeding strategies for premature infants: beneficial outcomes of feeding fortified human milk versus preterm formula. Pediatrics. 1999; 103(6):1150 –1157

6. Dewey KG, Heinig MJ, Nommsen-Rivers LA.

  Differences in morbidity between breast- fed and formula-fed infants. J Pediatr. 1995; 126(5):696 –702

  

15. Cooke RJ, Embleton ND. Feeding issues in

preterm infants. Arch Dis Child Fetal Neona- tal Ed. 2000;83(3):F215–F218

  7. Furman L, Taylor G, Minich N, Hack M. The effect of maternal milk on neonatal morbid- ity of very low birth weight infants. Arch Pe- diatr Adolesc Med. 2003;157(1):66 –71

  8. Valentine CJ, Hurst NM, Schanler RJ. Hind- milk improves weight gain in low birth weight infants fed human milk. J Pediatr Gastroenterol Nutr. 1994;18(4):474 – 477

  9. Dvorak B, Halpern MD, Holubec H, et al. Ma- ternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr Res. 2003; 53(3):426 – 433

  10. Lucas A, Morley R, Cole TJ, Gore SM. A ran- domized multicentre study of human milk versus formula and later development in preterm infants. Arch Dis Child Fetal Neona- tal Ed. 1994;70(2):F141–F146

  11. Eidelman AI, Feldman R. Positive effect of human milk on neurobehavioral and cogni- tive development of premature infants. Adv Exp Med Biol. 2004;554:359 –364

  12. Furman L, Minich N, Hack M. Correlates of lac- tation in mothers of very low birth weight in- fants. Pediatrics. 2002;109(4). Available at: www.pediatrics.org/cgi/content/full/109/4/ e57

  

13. Aguayo J. Maternal lactation for preterm

newborn infants. Early Hum Dev. 2001; 65(suppl):S19 –S29

  

14. Meier P, Brown LP. State of the science:

breastfeeding for mothers and low birth weight infants. Nurs Clin North Am. 1996; 31(2):351–365

23. Lucas A, Gibbs JA, Lyster RL, Baum JD.

  

Energy Expenditure for Breastfeeding and Bottle-Feeding Preterm Infants

Irit Berger, Valentin Weintraub, Shaul Dollberg, Rozalia Kopolovitz and Dror Mandel

  Pediatrics 2009;124;e1149-e1152; originally published online Nov 23, 2009;

DOI: 10.1542/peds.2009-0165

  Updated Information including high-resolution figures, can be found at: & Services

References This article cites 33 articles, 10 of which you can access for free

at:

  Citations This article has been cited by 1 HighWire-hosted articles: http://www.pediatrics.org/cgi/content/full/124/6/e1149#otherarti

  Subspecialty Collections This article, along with others on similar topics, appears in the following collection(s): Nutrition & Metabolism http://www.pediatrics.org/cgi/collection/nutrition_and_metabolis

  Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at:

  Reprints Information about ordering reprints can be found online: