Infant formula composition affects energetic efficiency for growth: The BeMIM study, a randomized controlled trial

Clinical Nutrition

Volumn 33, Issue 4, 2014, Pages 588-595

  Fleddermann, Manja ^a   Demmelmair, Hans ^a   Grote, Veit ^a   Nikolic, Tatjana ^b   Trisic, Branka ^c   Koletzko, Berthold ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b CLINICAL CENTER OF SERBIA   (Serbia)

^c HiPP Study Center   (Serbia)

Author keywords

Alpha lactalbumin; Fully formula fed; Growth; Infant formula; Low protein

Indexed keywords

ALBUMIN; ALPHA LACTALBUMIN; CARBOHYDRATE; CASEIN; CREATININE; GLYCEROPHOSPHOLIPID; LIPID; LONG CHAIN FATTY ACID; POLYUNSATURATED FATTY ACID; PROTEIN; UREA; LACTALBUMIN; PROTEIN INTAKE; UNSATURATED FATTY ACID;

ANTHROPOMETRY; ARTICLE; ARTIFICIAL MILK; CALORIC INTAKE; CHILD GROWTH; CONTROLLED STUDY; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; EDUCATION; ENERGY CONSERVATION; ENERGY METABOLISM; FOOD COMPOSITION; GESTATIONAL AGE; HEAD CIRCUMFERENCE; HUMAN; HUMAN EXPERIMENT; INFANT; MATERNAL AGE; NORMAL HUMAN; NUTRITIONAL ASSESSMENT; PROTEIN CONTENT; RANDOMIZED CONTROLLED TRIAL; VENOUS BLOOD; WHEY; ADMINISTRATION AND DOSAGE; ANALYSIS; BREAST MILK; CHEMISTRY; INFANT NUTRITION; INTERVENTION STUDY; NEWBORN; PROTEIN INTAKE; SATIETY; WEIGHT GAIN;

DIETARY PROTEINS; DOUBLE-BLIND METHOD; ENERGY INTAKE; FATTY ACIDS, UNSATURATED; HUMANS; INFANT FORMULA; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; INFANT, NEWBORN; INTERVENTION STUDIES; LACTALBUMIN; MILK, HUMAN; SATIATION; WEIGHT GAIN;

EID: 84902383811     PISSN: 02615614     EISSN: 15321983     Source Type: Journal    
DOI: 10.1016/j.clnu.2013.12.007     Document Type: Article

References (53)

1. World Health Organization (WHO) The optimal duration of exclusive breastfeeding 2001, Report of an expert consultation. Genf, 2001 (document WHO/NHD/01.09, WHO/FCH/CAH/01.24).
2. Kramer M.S., Kakuma R. Optimal duration of exclusive breastfeeding. Cochrane Database Syst Rev 2012, 8:CD003517.
3. Koletzko B., von Kries R., Close-Monasterolo R., Subías J.E., Scaglioni S., Giovannini M., et al. Can infant feeding choices modulate later obesity risk?. Am J Clin Nutr 2009, 89:1502S-1508S.
4. Robinson S., Fall C. Infant nutrition and later health: a review of current evidence. Nutrients 2012, 4:859-874.
5. Koletzko B., Baker S., Cleghorn G., Neto U.F., Gopalan S., Hernell O., et al. Global standard for the composition of infant formula: recommendations of an ESPGHAN coordinated international expert group. JPediatr Gastroenterol Nutr 2005, 41:584-599.
6. Fleith M., Clandinin M.T. Dietary PUFA for preterm and term infants: review of clinical studies. Crit Rev Food Sci Nutr 2005, 45:205-229.
7. Koletzko B., von Kries R., Closa-Monasterolo R., Escribano J., Scaglioni S., Giovannini M., et al. Lower protein in infant formula is associated with lower weight up to age two years: a randomized clinical trial. Am J Clin Nutr 2009, 89:1-10.
8. Lien E.L., Davis A.M., Euler A.R., the Multicenter Study Group Growth and safety in term infants fed reduced-protein formula with added bovine alpha-lactalbumin. JPediatr Gastroenterol Nutr 2004, 38:170-176.
9. Alexy U., Kersting M., Sichert-Hellert W., Manz F., Schoech G. Energy intake and growth of 3- to 36-month-old German infants and children. Ann Nutr Metab 1999, 43:14-22.
10. Macé K., Steenhout P., Klassen P., Donnet A. Protein quality and quantity in cow's milk-based formula for healthy term infants: past, present and future. Nestle Nutr Workshop Ser Pediatr Program 2006, 58:189-205.
11. Axelsson I. Effects of high protein intakes. Nestle Nutr Workshop Ser Pediatr Program 2006, 58:121-131.
12. Socha P., Grote V., Gruszfeld D., Janas R., Demmelmair H., Closa-Monasterolo, et al. Milk protein intake, the metabolic-endocrine response, and growth in infancy: data from a randomized clinical trial. Am J Clin Nutr 2011, 94:1776S-1784S.
13. Leunissen R.W., Kerkhof G.F., Stijnen T., Hokken-Koelega A. Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic risk profile in early adulthood. JAm Med Assoc 2009, 301:2234-2242.
14. Davis A.M., Harris B.J., Lien E.L., Pramuk K., Trabulsi J. Alpha-lactalbumin-rich infant formula fed to healthy term infants in a multicenter study: plasma essential amino acids and gastrointestinal tolerance. Eur J Clin Nutr 2008, 62:1294-1301.
15. Wurtman R.J., Wurtman J.J. Do carbohydrates affect food intake via neurotransmitter activity?. Appetite 1988, 11(Suppl.1):42-47.
16. Lönnerdal B., Lien L.E. Nutritional and physiologic significance of α-lactalbumin in infants. Nutr Rev 2003, 61:295-305.
17. Butte N.F., Smith E.O., Garza C. Energy utilization of breast-fed and formula-fed infants. Am J Clin Nutr 1990, 51:350-358.
18. Agostoni C. Role of long-chain polyunsaturated fatty acids in the first year of life. JPediatr Gastroenterol Nutr 2008, 47:S41-S44.
19. Koletzko B., Agostini C., Bergmann R., Ritzenthaler K., Shamir R. Physiological aspects of human milk lipids and implication for infant feeding: a workshop report. Acta Pediatr 2011, 100:1405-1415.
20. Massiera F., Saint-Marc P., Seydoux J., Murata T., Kobayashi T., Narumiya S., et al. Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern?. JLipid Res 2003, 44:271-279.
21. Sellmayer A., Koletzko B. Polyunsaturated fatty acids and eicosanoids in infants - physiological and pathophysiological aspects and open questions. Lipids 1999, 34:199-205.
22. Koletzko B., Shamir R., Ashwell M. Quality and safety aspects of infant nutrition. Ann Nutr Metab 2012, 60:179-184. Early Nutrition Academy (ENA), European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN)European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN).
23. Räihä N.C., Fazzolari-Nesci A., Cajozzo C., Puccio G., Monestier A., Moro G., et al. Whey predominant, whey modified infant formula with protein/energy ratio of 1.8g/100kcal: adequate and safe for term infants from birth to four months. JPediatr Gastroenterol Nutr 2002, 35:275-281.
24. Turck D., Grillon C., Lachambre E., Robiliard P., Beck L., Maurin J.L., et al. Adequacy and safety of an infant formula with a protein/energy ratio of 1.8g/100kcal and enhanced protein efficiency for term infants during the first 4 months of life. JPediatr Gastroenterol Nutr 2006, 43:365-371.
25. Fomon S.J., Ziegler E.E., Nelson S.E., Frantz J.A. What is the safe protein-energy ratio for infant formula. Am J Clin Nutr 1995, 62:358-363.
26. WHO Multicentre Growth Reference Study Group WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development 2006, World Health Organization, Geneva.
27. Haschke F., van't Hof M.A., Euro-Growth Study Group Euro-growth references for length, weight, and body circumferences. JPediatr Gastroenterol Nutr 2000, 31:S14-S38.
28. Commission Directive 2006/141/EC of 22 December 2006 on infant formulae and follow-on formulae and amending Directive 1999/21/EC p. L 401/2.
29. Commission Directive 1999/21/EC on infant formulae and follow-on formulae.
30. Harder U., Koletzko B., Peissner W. Quantification of 22 plasma amino acids combining derivatization and ion-pair LC-MS/MS. JChromatogr B Analyt Technol Biomed Life Sci 2011, 879:495-504.
31. Glaser C., Demmelmair H., Koletzko B. High-throughput analysis of fatty acid composition of plasma glycerophospholipids. JLipid Res 2010, 51:216-221.
32. Glaser C., Demmelmair H., Sausenthaler A., Herbarth O., Heinrich J., Koletzko B. Fatty acid composition of serum glycerophospholipids in children. JPediatr 2010, 157:826-831.
33. Trabulsi J., Capeding R., Lebumfacil J., Ramanujam K., Feng P., McSweeney, et al. Effect of an α-lactalbumin-enriched infant formula with lower protein on growth. Eur J Clin Nutr 2011, 65:167-174.
34. Fomon S.J., Ziegler E.E., Nelson S.E., Rogers R.R., Frantz J.A. Infant formula with protein-energy ratio of 1.7g/100kcal is adequate but may not be safe. JPediatr Gastroenterol Nutr 1999, 28:495-501.
35. Ziegler E.E. Growth of breast-fed and formula-fed infants. Nestle Nutr Workshop Ser Pediatr Program 2006, 58:51-63.
36. Hanning R.M., Paes B., Atkinson S.A. Protein metabolism and growth of term infants in response to a reduced-protein, 40:60 whey: casein formula with added tryptophan. Am J Clin Nutr 1992, 56:1004-1011.
37. Lien E.L. Infant formulas with increased concentrations of alpha-lactalbumin. Am J Clin Nutr 2003, 77:1555S-1558S.
38. Halford J.C., Harrold J.A., Lawton C.L., Blundell J.E. Serotonin (5-HT) drugs: effects on appetite expression and use for the treatment of obesity. Curr Drug Targets 2005, 6:201-213.
39. Lindquist S., Hernell O. Lipid digestion and absorption in early life: an update. Curr Opin Clin Nutr Metab Care 2010, 13:314-320.
40. Koletzko B., Rodriguez-Palmero M., Demmelmair H., Fidler N., Jensen R., Sauerwald T. Physiological aspects of human milk lipids. Early Hum Dev 2001, 65:S3-S18.
41. Amate L., Gil A., Ramirez M. Feeding infant piglets formula with long-chain polyunsaturated fatty acids as triacylglycerols or phospholipids influences the distribution of these fatty acids in plasma lipoprotein fractions. JNutr 2001, 131:1250-1255.
42. Sala-Vila A., Castellote A.I., Campoy C., Rivero M., Rodriguez-Palmero M., Lopez-Sabater M.C. The source of long-chain PUFA in formula supplements does not affect the fatty acid composition of plasma lipids in full-term infants. JNutr 2004, 134:868-873.
43. Carlson S.E., Werkman S.H., Peeples J.M., Cooke R.J., Tolley E.A. Arachidonic acid status correlates with first year growth in preterm infants. Proc Natl Acad Sci U S A 1993, 90:1073-1077.
44. Campoy C., Escolano-Margarit M.V., Anjos T., Szajewska H., Uauy R. Omega 3 fatty acids on child growth, visual acuity and neurodevelopment. Br J Nutr 2012, 107:S85-S106.
45. Auestad N., Halter R., Hall R.T., Blatter M., Bogle M.L., Burks W., et al. Growth and development in term infants fed long-chain polyunsaturated fatty acids: a double-masked, randomized, parallel, prospective, multivariate study. Pediatrics 2001, 108:372-381.
46. Arenz S., Rückerl R., Koletzko B., von Kries R. Breastfeeding and childhood obesity - a systematic review. Int J Obes 2004, 28:1247-1256.
47. Harder T., Bergmann R., Kallischnigg G., Plagemann A. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 2005, 162:397-403.
48. Weng S.F., Redsell S.A., Swift J.A., Yang M., Glazebrook C.P. Systematic review and meta-analyses of risk factors for childhood overweight identifiable during infancy. Arch Dis Child 2012, 97:1019-1026.
49. Günther A.L.B., Buyken A.E., Kroke A. The influence of habitual protein intake in early childhood on BMI and age at adiposity rebound: results from the DONALD Study. Int J Obes 2006, 30:1072-1079.
50. Young B.E., Johnson S.L., Krebs N.F. Biological determinants linking infant weight gain and child obesity: current knowledge and future directions. Adv Nutr 2012, 3:675-686.
51. Koletzko B., Brands B., Poston L., Godfrey K., Demmelmair H., Early Nutrition Project Early nutrition programming of long-term health. Proc Nutr Soc 2012, 71:371-378.
52. Nommsen L.A., Lovelady C.A., Heinig M.J., Loennerdal, Dewey K.G. Determinants of energy, protein, lipid, and lactose concentrations in human milk during the first 12mo of lactation: the DARLING Study. Am J Clin Nutr 1991, 53:457-465.
53. Food and Nutrition Board Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids 2001, The National Academies Press, Washington.