{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,26]],"date-time":"2026-06-26T20:59:26Z","timestamp":1782507566853,"version":"3.54.5"},"reference-count":43,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,11,6]],"date-time":"2021-11-06T00:00:00Z","timestamp":1636156800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>The nutritional management of preterm infants is a critical point of care, especially because of the increased risk of developing extrauterine growth restriction (EUGR), which is associated with worsened health outcomes. Energy requirements in preterm infants are simply estimated, so the measurement of resting energy expenditure (REE) should be a key point in the nutritional evaluation of preterm infants. Although predictive formulae are available, it is well known that they are imprecise. The aim of our study was the evaluation of REE and protein oxidation (Ox) in very low birth weight infants (VLBWI) and the association with the mode of feeding and with body composition at term corrected age. Methods: Indirect calorimetry and body composition were performed at term corrected age in stable very low birth weight infants. Urinary nitrogen was measured in spot urine samples to calculate Ox. Infants were categorized as prevalent human milk (HMF) or prevalent formula diet (PFF). Results: Fifty VLBWI (HMF: 23, PFF: 27) were evaluated at 36.48 \u00b1 0.85 post-conceptional weeks. No significant differences were found in basic characteristics or nutritional intake in the groups at birth and at the assessment. No differences were found in the REE of HMF vs. PFF (59.69 \u00b1 9.8 kcal\/kg\/day vs. 59.27 \u00b1 13.15 kcal\/kg\/day, respectively). We found statistical differences in the protein-Ox of HMF vs. PFF (1.7 \u00b1 0.92 g\/kg\/day vs. 2.8 \u00b1 1.65 g\/kg\/day, respectively, p &lt; 0.01), and HMF infants had a higher fat-free mass (kg) than PFF infants (2.05 \u00b1 0.26 kg vs. 1.82 \u00b1 0.35 kg, respectively, p &lt; 0.01), measured with air displacement plethysmography. Conclusion: REE is similar in infants with a prevalent human milk diet and in infants fed with formula. The HMF infants showed a lower oxidation rate of proteins for energy purposes and a better quality of growth. A greater amount of protein in HMF is probably used for anabolism and fat-free mass deposition. Further studies are needed to confirm our hypothesis.<\/jats:p>","DOI":"10.3390\/nu13113962","type":"journal-article","created":{"date-parts":[[2021,11,7]],"date-time":"2021-11-07T20:42:54Z","timestamp":1636317774000},"page":"3962","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Energy Expenditure, Protein Oxidation and Body Composition in a Cohort of Very Low Birth Weight Infants"],"prefix":"10.3390","volume":"13","author":[{"given":"Michela","family":"Perrone","sequence":"first","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Camilla","family":"Menis","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"},{"name":"Department of Clinical Sciences and Community Health, University of Milan, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pasqua","family":"Piemontese","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Tabasso","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Domenica","family":"Mallardi","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Orsi","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Orsola","family":"Amato","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0425-5046","authenticated-orcid":false,"given":"Nadia","family":"Liotto","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2667-4620","authenticated-orcid":false,"given":"Paola","family":"Roggero","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"},{"name":"Department of Clinical Sciences and Community Health, University of Milan, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabio","family":"Mosca","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Fondazione IRCCS Ca\u2019 Granda Ospedale Maggiore Policlinico, 20122 Milan, Italy"},{"name":"Department of Clinical Sciences and Community Health, University of Milan, 20122 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,6]]},"reference":[{"key":"ref_1","first-page":"395","article-title":"Nutritional Needs of Infants","volume":"60","author":"Clement","year":"2015","journal-title":"Textb. Nutr. Diet. Post Basic BSc Nurs. Stud."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e20172467","DOI":"10.1542\/peds.2017-2467","article-title":"Monitoring the postnatal growth of preterm infants: A paradigm change","volume":"141","author":"Villar","year":"2018","journal-title":"Pediatrics"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1136\/adc.2009.175067","article-title":"Conceptual issues related to the construction of prescriptive standards for the evaluation of postnatal growth of preterm infants","volume":"95","author":"Villar","year":"2010","journal-title":"Arch. Dis. Child."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Tan, J.B.C., Boskovic, D.S., and Angeles, D.M. (2018). The energy costs of prematurity and the neonatal intensive care unit (NICU) experience. Antioxidants, 7.","DOI":"10.3390\/antiox7030037"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Peila, C., Spada, E., Giuliani, F., Maiocco, G., Raia, M., Cresi, F., Bertino, E., and Coscia, A. (2020). Extrauterine growth restriction: Definitions and predictability of outcomes in a cohort of very low birth weight infants or preterm neonates. Nutrients, 12.","DOI":"10.3390\/nu12051224"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e84","DOI":"10.1542\/peds.2015-0129","article-title":"Weight growth velocity and postnatal growth failure in infants 501 to 1500 Grams: 2000\u20132013","volume":"136","author":"Horbar","year":"2015","journal-title":"Pediatrics"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1038\/jp.2016.85","article-title":"Growth failure among preterm infants due to insufficient protein is not innocuous and must be prevented","volume":"36","author":"Hay","year":"2016","journal-title":"J. Perinatol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.arcped.2020.02.003","article-title":"Mortality and morbidity of preterm neonates weighing less than 750 g: A 2-year retrospective cohort study","volume":"27","author":"Carriere","year":"2020","journal-title":"Arch. Pediatr."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e645","DOI":"10.1542\/neo.19-11-e645","article-title":"Enteral feeding of the preterm infant","volume":"19","author":"Brune","year":"2018","journal-title":"Neoreviews"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1007\/s00431-020-03628-1","article-title":"Extrauterine growth restriction in very preterm infant: Etiology, diagnosis, and 2-year follow-up","volume":"179","year":"2020","journal-title":"Eur. J. Pediatr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.jpeds.2016.03.003","article-title":"Greater early gains in fat-free mass, but not fat mass, are associated with improved neurodevelopment at 1 year corrected age for prematurity in very low birth weight preterm infants","volume":"173","author":"Ramel","year":"2016","journal-title":"J. Pediatr."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Cormack, B.E., Harding, J.E., Miller, S.P., and Bloomfield, F.H. (2019). The influence of early nutrition on brain growth and neurodevelopment in extremely preterm babies: A narrative review. Nutrients, 11.","DOI":"10.3390\/nu11092029"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/1476-069X-11-42","article-title":"Developmental origins of non-communicable disease: Implications for research and public health","volume":"11","author":"Barouki","year":"2012","journal-title":"Environ. Health"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1093\/ajcn\/nqx001","article-title":"Protein use and weight-gain quality in very-low-birth-weight preterm infants fed human milk or formula","volume":"107","author":"Morlacchi","year":"2018","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Giann\u00ec, M.L., Consonni, D., Liotto, N., Roggero, P., Morlacchi, L., Piemontese, P., Menis, C., and Mosca, F. (2016). Does human milk modulate body composition in late preterm infants at term-corrected age?. Nutrients, 8.","DOI":"10.3390\/nu8100664"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1093\/ajcn\/67.1.74","article-title":"Resting energy expenditure in children in a pediatric intensive care unit: Comparison of Harris-Benedict and Talbot predictions with indirect calorimetry values","volume":"67","author":"Jefferson","year":"1998","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1097\/MPG.0000000000001223","article-title":"Accuracy of prediction formulae for the assessment of resting energy expenditure in hospitalized children","volume":"63","author":"Agostoni","year":"2016","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/S0095-5108(05)70013-0","article-title":"Energy expenditure in the extremely low-birth weight infant","volume":"27","author":"Leitch","year":"2000","journal-title":"Clin. Perinatol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"111180","DOI":"10.1016\/j.nut.2021.111180","article-title":"The indirect calorimetry in very low birth weight preterm infants: An easier and reliable procedure","volume":"86","author":"Perrone","year":"2021","journal-title":"Nutrition"},{"key":"ref_20","first-page":"628","article-title":"Calculation of substrate oxidation rates in vivo from gaseous exchange","volume":"121","author":"Frayn","year":"2016","journal-title":"J. Appl. Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1097\/00000658-198001000-00008","article-title":"Influence of total parenteral nutrition on fuel utilization in injury and sepsis","volume":"191","author":"Askanazi","year":"1980","journal-title":"Ann. Surg."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1002\/bjs.1800700113","article-title":"The effect of sepsis on the oxidation of carbohydrate and fat","volume":"70","author":"Stoner","year":"1983","journal-title":"Br. J. Surg."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1203\/00006450-198607000-00012","article-title":"Energy balance, physical activity, and thermogenic effect of feeding in premature infants","volume":"20","author":"Freymond","year":"1986","journal-title":"Pediatr. Res."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Roggero, P., Giann\u00ec, M.L., Orsi, A., Amato, O., Piemontese, P., Liotto, N., Morlacchi, L., Taroni, F., Garavaglia, E., and Bracco, B. (2012). Implementation of Nutritional Strategies Decreases Postnatal Growth Restriction in Preterm Infants. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0051166"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1097\/MPG.0b013e3181adaee0","article-title":"Enteral nutrient supply for preterm infants: Commentary from the european society of paediatric gastroenterology, hepatology and nutrition committee on nutrition","volume":"50","author":"Agostoni","year":"2010","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1186\/s12967-016-0957-y","article-title":"Is targeted fortification of human breast milk an optimal nutrition strategy for preterm infants? An interventional study","volume":"14","author":"Morlacchi","year":"2016","journal-title":"J. Transl. Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1136\/archdischild-2018-315006","article-title":"Growth of preterm infants at the time of global obesity","volume":"104","author":"Villar","year":"2019","journal-title":"Arch. Dis. Child."},{"key":"ref_28","unstructured":"The International Fetal and Newborn Growth Consortium (2012). International Fetal and Newborn Growth Standards for the 21st Century Anthropometry Handbook, The International Fetal and Newborn Growth Consortium."},{"key":"ref_29","unstructured":"(2021, September 21). The INTERGROWTH-21st Project. Available online: http:\/\/intergrowth21.ndog.ox.ac.uk."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1113\/jphysiol.1949.sp004363","article-title":"New methods for calculating metabolic rate with special reference to protein metabolism","volume":"109","author":"Weir","year":"1949","journal-title":"J. Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1177\/014860710302700121","article-title":"Clinical use of the respiratory quotient obtained from indirect calorimetry","volume":"27","author":"McClave","year":"2003","journal-title":"J. Parenter. Enter. Nutr."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1111\/j.1651-2227.1997.tb08923.x","article-title":"Measurement of albumin and low molecular weight proteins in the urine of newborn infants using a cotton wool ball collection method","volume":"86","author":"Fell","year":"1997","journal-title":"Acta Paediatr. Int. J. Paediatr."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1038\/pr.2012.75","article-title":"Evaluation of air-displacement plethysmography for body composition assessment in preterm infants","volume":"72","author":"Roggero","year":"2012","journal-title":"Pediatr. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1203\/01.PDR.0000049669.74793.E3","article-title":"A new air displacement plethysmograph for the measurement of body composition in infants","volume":"53","author":"Urlando","year":"2003","journal-title":"Pediatr. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.1093\/ajcn\/35.5.1169","article-title":"Body composition of reference children from birth to age 10 years","volume":"35","author":"Fomon","year":"1982","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1067\/S0022-3476(03)00532-8","article-title":"Energy expenditure in human milk- versus formula-fed preterm infants","volume":"143","author":"Lubetzky","year":"2003","journal-title":"J. Pediatr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1097\/MPG.0000000000001261","article-title":"Estimation of fat-free mass at discharge in preterm infants fed with optimized feeding regimen","volume":"64","author":"Larcade","year":"2017","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1017\/S0007114516001720","article-title":"Effects of breast-feeding compared with formula-feeding on preterm infant body composition: A systematic review and meta-analysis","volume":"116","author":"Huang","year":"2016","journal-title":"Br. J. Nutr."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jnutbio.2016.06.001","article-title":"Longitudinal evolution of true protein, amino acids and bioactive proteins in breast milk: A developmental perspective","volume":"41","author":"Erdmann","year":"2017","journal-title":"J. Nutr. Biochem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.nut.2019.04.002","article-title":"Differences in energy expenditure in human donor milk versus formula milk in preterm newborns: A crossover study","volume":"66","author":"Soares","year":"2019","journal-title":"Nutrition"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0022-3476(84)80368-6","article-title":"Nutrient balance, energy utilization, and composition of weight gain in very-low-birth-weight infants fed pooled human milk or a preterm formula","volume":"105","author":"Putet","year":"1984","journal-title":"J. Pediatr."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1203\/00006450-198311000-00011","article-title":"Energy balance and nitrogen balance in growing low birthweight infants fed human milk or formula","volume":"17","author":"Whyte","year":"1983","journal-title":"Pediatr. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"898","DOI":"10.1136\/adc.57.12.898","article-title":"Energy balance, nitrogen balance, and growth in preterm infants fed expressed breast milk, a premature infant formula, and two low-solute adapted formulae","volume":"57","author":"Brooke","year":"1982","journal-title":"Arch. Dis. Child."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/11\/3962\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:26:56Z","timestamp":1760167616000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/13\/11\/3962"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,6]]},"references-count":43,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["nu13113962"],"URL":"https:\/\/doi.org\/10.3390\/nu13113962","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,6]]}}}