Early weight measures and long-term neuropsychological outcome of critically ill neonates and infants: a secondary analysis of the PEPaNIC trial.
Anthropometrics
Infants
Neonates
Neuropsychology
Pediatric intensive care unit
Journal
European journal of pediatrics
ISSN: 1432-1076
Titre abrégé: Eur J Pediatr
Pays: Germany
ID NLM: 7603873
Informations de publication
Date de publication:
11 Nov 2023
11 Nov 2023
Historique:
received:
13
07
2023
accepted:
18
10
2023
revised:
17
10
2023
medline:
11
11
2023
pubmed:
11
11
2023
entrez:
11
11
2023
Statut:
aheadofprint
Résumé
Neonates and infants surviving critical illness show impaired growth during critical illness and are at risk for later neuropsychological impairments. Early identification of individuals most at risk is needed to provide tailored long-term follow-up and care. The research question is whether early growth during hospitalization is associated with growth and neuropsychological outcomes in neonates and infants after pediatric intensive care unit admission (PICU). This is a secondary analysis of the PEPaNIC trial. Weight measurements upon PICU admission, at PICU discharge, at hospital discharge, at 2- and 4-year follow-up, and of different subgroups were compared using (paired) t-tests. Multiple linear regression analyses were performed to investigate the association between early growth in weight measures and neuropsychological outcomes at 4-year follow-up. One hundred twenty-one infants were included, and median age upon admission was 21 days. Growth in weight per week was less than the age-appropriate norm, resulting in a decrease in weight-for-age Z-score during hospitalization. Weight is normalized at 2- and 4-year follow-up. Weight gain in kilograms per week and change in weight Z-score were not associated with neurodevelopmental outcome measures at 4-year follow-up. Lower weight-for-age Z-score at PICU admission and at hospital discharge was associated only with lower weight and height Z-scores at 4-year follow-up. Growth in weight during hospital stay of young survivors of critical illness is impaired. Worse early growth in weight is associated with lower weight and height but not with neuropsychological outcomes at 4-year follow-up. • Critically ill neonates and infants show impaired early growth during admission and are at risk for later neuropsychological impairments. • Unraveling the association between early growth and later neuropsychological impairments is crucial since the first year of life is critical for brain development. • Critically ill neonates and infants had age appropriate weight measures at 4-year follow-up. • Poor growth in weight during hospital stay was not associated with poorer cognitive, emotional, or behavioral functioning four years after critical illness.
Identifiants
pubmed: 37950792
doi: 10.1007/s00431-023-05298-1
pii: 10.1007/s00431-023-05298-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Vlaamse regering
ID : METH14/06
Organisme : Vlaamse regering
ID : METH/08/07
Organisme : FP7 Ideas: European Research Council
ID : AdvG-2012-321670
Organisme : Horizon 2020
ID : AdvG-2017-785809
Organisme : institute for science and technology
ID : IWT/070695/TBM
Informations de copyright
© 2023. The Author(s).
Références
Euro-Peristat Project. European Perinatal Health Report. Core indicators of the health and care of pregnant women and babies in Europe in 2015. November 2018. https://www.europeristat.com/
Broeders L, Achterberg PW, Waelput AJM, Ravelli ACJ, Kwee A, Groenendaal F, Offerhaus P, van der Velden K, Rosman AN, Nijhuis JG (2019) Decrease in foetal and neonatal mortality in the Netherlands; comparison with other Euro-Peristat countries in 2004, 2010 and 2015 Afname van foetale en neonatale sterfte in Nederland. Ned Tijdschr Geneeskd 163
White BR, Rogers LS, Kirschen MP (2019) Recent advances in our understanding of neurodevelopmental outcomes in congenital heart disease. Curr Opin Pediatr 31:783–788
pubmed: 31693588
pmcid: 6852883
doi: 10.1097/MOP.0000000000000829
Verstraete S, Van den Berghe G, Vanhorebeek I (2018) What’s new in the long-term neurodevelopmental outcome of critically ill children. Intensive Care Med 44:649–651
pubmed: 29063130
doi: 10.1007/s00134-017-4968-9
Bellinger DC, Wypij D, Rivkin MJ, DeMaso DR, Robertson RL Jr, Dunbar-Masterson C, Rappaport LA, Wernovsky G, Jonas RA, Newburger JW (2011) Adolescents with d-transposition of the great arteries corrected with the arterial switch procedure: neuropsychological assessment and structural brain imaging. Circulation 124:1361–1369
pubmed: 21875911
pmcid: 3217719
doi: 10.1161/CIRCULATIONAHA.111.026963
Goldberg CS, Lu M, Sleeper LA, Mahle WT, Gaynor JW, Williams IA, Mussatto KA, Ohye RG, Graham EM, Frank DU, Jacobs JP, Krawczeski C, Lambert L, Lewis A, Pemberton VL, Sananes R, Sood E, Wechsler SB, Bellinger DC, Newburger JW, Pediatric Heart Network I (2014) Factors associated with neurodevelopment for children with single ventricle lesions. J Pediatr 165(490–496):e498
Jacobs A, Dulfer K, Eveleens RD, Hordijk J, Van Cleemput H, Verlinden I, Wouters PJ, Mebis L, Guerra GG, Joosten K, Verbruggen SC, Guiza F, Vanhorebeek I, Van den Berghe G (2020) Long-term developmental effect of withholding parenteral nutrition in paediatric intensive care units: a 4-year follow-up of the PEPaNIC randomised controlled trial. Lancet Child Adolesc Health 4:503–514
pubmed: 32562632
doi: 10.1016/S2352-4642(20)30104-8
Verstraete S, Verbruggen SC, Hordijk JA, Vanhorebeek I, Dulfer K, Guiza F, van Puffelen E, Jacobs A, Leys S, Durt A, Van Cleemput H, Eveleens RD, Garcia Guerra G, Wouters PJ, Joosten KF, Van den Berghe G (2019) Long-term developmental effects of withholding parenteral nutrition for 1 week in the paediatric intensive care unit: a 2-year follow-up of the PEPaNIC international, randomised, controlled trial. Lancet Respir Med 7:141–153
pubmed: 30224325
doi: 10.1016/S2213-2600(18)30334-5
Madderom MJ, Reuser JJ, Utens EM, van Rosmalen J, Raets M, Govaert P, Steiner K, Gischler SJ, Tibboel D, van Heijst AF, Ijsselstijn H (2013) Neurodevelopmental, educational and behavioral outcome at 8 years after neonatal ECMO: a nationwide multicenter study. Intensive Care Med 39:1584–1593
pubmed: 23740280
doi: 10.1007/s00134-013-2973-1
Mesotten D, Gielen M, Sterken C, Claessens K, Hermans G, Vlasselaers D, Lemiere J, Lagae L, Gewillig M, Eyskens B, Vanhorebeek I, Wouters PJ, Van den Berghe G (2012) Neurocognitive development of children 4 years after critical illness and treatment with tight glucose control: a randomized controlled trial. JAMA 308:1641–1650
pubmed: 23101118
doi: 10.1001/jama.2012.12424
Newburger JW, Sleeper LA, Bellinger DC, Goldberg CS, Tabbutt S, Lu M, Mussatto KA, Williams IA, Gustafson KE, Mital S, Pike N, Sood E, Mahle WT, Cooper DS, Dunbar-Masterson C, Krawczeski CD, Lewis A, Menon SC, Pemberton VL, Ravishankar C, Atz TW, Ohye RG, Gaynor JW, Pediatric Heart Network I (2012) Early developmental outcome in children with hypoplastic left heart syndrome and related anomalies: the single ventricle reconstruction trial. Circulation 125:2081–2091
pubmed: 22456475
pmcid: 3341507
doi: 10.1161/CIRCULATIONAHA.111.064113
Hordijk JA, Verbruggen SC, Buysse CM, Utens EM, Joosten KF, Dulfer K (2022) Neurocognitive functioning and health-related quality of life of children after pediatric intensive care admission: a systematic review. Qual Life Res 31(9):2601–2614
pubmed: 35357629
pmcid: 9356943
doi: 10.1007/s11136-022-03124-z
Marino BS, Lipkin PH, Newburger JW, Peacock G, Gerdes M, Gaynor JW, Mussatto KA, Uzark K, Goldberg CS, Johnson WH Jr, Li J, Smith SE, Bellinger DC, Mahle WT, American Heart Association Congenital Heart Defects Committee CoCDitYCoCN, Stroke C (2012) Neurodevelopmental outcomes in children with congenital heart disease: evaluation and management: a scientific statement from the American Heart Association. Circulation 126:1143–1172
pubmed: 22851541
doi: 10.1161/CIR.0b013e318265ee8a
Sterken C, Lemiere J, Vanhorebeek I, Van den Berghe G, Mesotten D (2015) Neurocognition after paediatric heart surgery: a systematic review and meta-analysis. Open Heart 2:e000255
pubmed: 26568832
pmcid: 4636679
doi: 10.1136/openhrt-2015-000255
Schiller R, Ijsselstijn H, Hoskote A, White T, Verhulst F, van Heijst A, Tibboel D (2018) Memory deficits following neonatal critical illness: a common neurodevelopmental pathway. Lancet Child Adolesc Health 2:281–289
Anderson PJ (2014) Neuropsychological outcomes of children born very preterm. Semin Fetal Neonatal Med 19:90–96
pubmed: 24361279
doi: 10.1016/j.siny.2013.11.012
Hulst J, Joosten K, Zimmermann L, Hop W, van Buuren S, Buller H, Tibboel D, van Goudoever J (2004) Malnutrition in critically ill children: from admission to 6 months after discharge. Clin Nutr 23:223–232
pubmed: 15030962
doi: 10.1016/S0261-5614(03)00130-4
Bairdain S, Khan FA, Fisher J, Zurakowski D, Ariagno K, Cauley RP, Zalieckas J, Wilson JM, Jaksic T, Mehta NM (2015) Nutritional outcomes in survivors of congenital diaphragmatic hernia (CDH)-factors associated with growth at one year. J Pediatr Surg 50:74–77
pubmed: 25598097
doi: 10.1016/j.jpedsurg.2014.10.003
Eskedal LT, Hagemo PS, Seem E, Eskild A, Cvancarova M, Seiler S, Thaulow E (2008) Impaired weight gain predicts risk of late death after surgery for congenital heart defects. Arch Dis Child 93:495–501
pubmed: 18230653
doi: 10.1136/adc.2007.126219
Karpen HE (2016) Nutrition in the cardiac newborns: evidence-based nutrition guidelines for cardiac newborns. Clin Perinatol 43:131–145
pubmed: 26876126
doi: 10.1016/j.clp.2015.11.009
Hulst JM, van Goudoever JB, Zimmermann LJ, Hop WC, Albers MJ, Tibboel D, Joosten KF (2004) The effect of cumulative energy and protein deficiency on anthropometric parameters in a pediatric ICU population. Clin Nutr 23:1381–1389
pubmed: 15556260
doi: 10.1016/j.clnu.2004.05.006
Kaufman J, Vichayavilas P, Rannie M, Peyton C, Carpenter E, Hull D, Alpern J, Barrett C, da Cruz EM, Roosevelt G (2015) Improved nutrition delivery and nutrition status in critically ill children with heart disease. Pediatrics 135:e717–725
Ross FJ, Radman M, Jacobs ML, Sassano-Miguel C, Joffe DC, Hill KD, Chiswell K, Feng L, Jacobs JP, Vener DF, Latham GJ (2020) Associations between anthropometric indices and outcomes of congenital heart operations in infants and young children: an analysis of data from the Society of Thoracic Surgeons Database. Am Heart J 224:85–97
pubmed: 32353587
doi: 10.1016/j.ahj.2020.03.012
van Puffelen E, Hulst JM, Vanhorebeek I, Dulfer K, Van den Berghe G, Joosten KFM, Verbruggen S (2020) Effect of late versus early initiation of parenteral nutrition on weight deterioration during PICU stay: secondary analysis of the PEPaNIC randomised controlled trial. Clin Nutr 39:104–109
pubmed: 30879734
doi: 10.1016/j.clnu.2019.02.014
Bhutta ZA, Guerrant RL, Nelson CA 3rd (2017) Neurodevelopment, nutrition, and inflammation: the evolving global child health landscape. Pediatrics 139:S12–S22
pubmed: 28562245
doi: 10.1542/peds.2016-2828D
Fox SE, Levitt P, Nelson CA 3rd (2010) How the timing and quality of early experiences influence the development of brain architecture. Child Dev 81:28–40
pubmed: 20331653
pmcid: 2846084
doi: 10.1111/j.1467-8624.2009.01380.x
Kolb B, Fantie BD (2009) Development of the child’s brain and behavior. Handbook of clinical child neuropsychology. Springer Science + Business Media, New York, pp 19–46
Knickmeyer RC, Gouttard S, Kang C, Evans D, Wilber K, Smith JK, Hamer RM, Lin W, Gerig G, Gilmore JH (2008) A structural MRI study of human brain development from birth to 2 years. J Neurosci 28:12176–12182
pubmed: 19020011
pmcid: 2884385
doi: 10.1523/JNEUROSCI.3479-08.2008
Claessens NHP, Kelly CJ, Counsell SJ, Benders M (2017) Neuroimaging, cardiovascular physiology, and functional outcomes in infants with congenital heart disease. Dev Med Child Neurol 59:894–902
pubmed: 28542743
doi: 10.1111/dmcn.13461
Ortinau CM, Shimony JS (2020) The congenital heart disease brain: prenatal considerations for perioperative neurocritical care. Pediatr Neurol 108:23–30
pubmed: 32107137
pmcid: 7306416
doi: 10.1016/j.pediatrneurol.2020.01.002
Peyvandi S, Latal B, Miller SP, McQuillen PS (2019) The neonatal brain in critical congenital heart disease: insights and future directions. Neuroimage 185:776–782
pubmed: 29787864
doi: 10.1016/j.neuroimage.2018.05.045
Fivez T, Kerklaan D, Verbruggen S, Vanhorebeek I, Verstraete S, Tibboel D, Guerra GG, Wouters PJ, Joffe A, Joosten K, Mesotten D, Van den Berghe G (2015) Impact of withholding early parenteral nutrition completing enteral nutrition in pediatric critically ill patients (PEPaNIC trial): study protocol for a randomized controlled trial. Trials 16:202
pubmed: 25927936
pmcid: 4422419
doi: 10.1186/s13063-015-0728-8
Fivez T, Kerklaan D, Mesotten D, Verbruggen S, Wouters PJ, Vanhorebeek I, Debaveye Y, Vlasselaers D, Desmet L, Casaer MP, Garcia Guerra G, Hanot J, Joffe A, Tibboel D, Joosten K, Van den Berghe G (2016) Early versus late parenteral nutrition in critically ill children. N Engl J Med 374:1111–1122
pubmed: 26975590
doi: 10.1056/NEJMoa1514762
Verlinden I, Dulfer K, Vanhorebeek I, Guiza F, Hordijk JA, Wouters PJ, Guerra GG, Joosten KF, Verbruggen SC, Van den Berghe G (2021) Role of age of critically ill children at time of exposure to early or late parenteral nutrition in determining the impact hereof on long-term neurocognitive development: a secondary analysis of the PEPaNIC-RCT. Clin Nutr 40:1005–1012
pubmed: 32758384
pmcid: 7957365
doi: 10.1016/j.clnu.2020.07.004
Kindergeneeskunde NVV (2021) Ondervoeding bij kinderen. p 42
Dubey AP (2015) Pediatric nutrition in practice, 2nd edn. Karger
Talma H (2010) Groeidiagrammen TNO (Dutch Growth Standards). https://www.tno.nl/nl/gezond/werk-jeugd-gezondheid/jeugd/eerste-1000-dagen-kind/groeidiagrammen-groeicalculators/
Fenton TR, Kim JH (2013) A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr 13:59
pubmed: 23601190
pmcid: 3637477
doi: 10.1186/1471-2431-13-59
van der Heijden KB, Suurland J, De Sonneville LM, Swaab HJ (2013) BRIEF-P: Vragenlijst executieve functies voor 2- tot 5-jarigen - Handleiding. Hogrefe, Amsterdam
Achenbach TM, Rescorla LA (2000) Manual for the ASEBA preschool forms and profiles. University of Vermont, Research Center for Children, Youth and Families, Burlington, VT
Hendriksen JG, Hurks PP (2010) WPPSI-III-NL Wechsler preschool and primary scale of intelligence. Nederlandstalige bewerking: handleiding. Pearson, Amsterdam
Hurks PP, Hendriksen JG, Dek J, Kooij A (2010) De nieuwe Wechsler kleuterintelligentietest voor 2:6–7:11 jarigen. Tijdschrift voor Neuropsychologie 2:40–51
Beery KEB, Beery NA (2010) The Beery-Buktenica developmental test of visual-motor integration, 6th edition (BEERY
De Sonneville LMJ (2005) Amsterdamse Neuropsychologische Taken: Wetenschappelijke en klinische toepassingen [Amsterdam neuropsychological tasks: scientific and clinical applications]. Tijdschrift voor Neuropsychologie 0:27–41
RStudio Team (2015) RStudio: integrated development environment for R [Internet]. Boston, MA
Pollack MM, Wiley JS, Holbrook PR (1981) Early nutritional depletion in critically ill children. Crit Care Med 9:580–583
pubmed: 6790227
doi: 10.1097/00003246-198108000-00005
Valla FV, Berthiller J, Gaillard-Le-Roux B, Ford-Chessel C, Ginhoux T, Rooze S, Cour-Andlauer F, Meyer R, Javouhey E (2018) Faltering growth in the critically ill child: prevalence, risk factors, and impaired outcome. Eur J Pediatr 177:345–353
pubmed: 29243190
doi: 10.1007/s00431-017-3062-1
Grippa RB, Silva PS, Barbosa E, Bresolin NL, Mehta NM, Moreno YM (2017) Nutritional status as a predictor of duration of mechanical ventilation in critically ill children. Nutrition 33:91–95
pubmed: 27364223
doi: 10.1016/j.nut.2016.05.002
Bagri NK, Jose B, Shah SK, Bhutia TD, Kabra SK, Lodha R (2015) Impact of malnutrition on the outcome of critically ill children. Indian J Pediatr 82:601–605
pubmed: 25804317
doi: 10.1007/s12098-015-1738-y
de Souza MF, Leite HP, Koch Nogueira PC (2012) Malnutrition as an independent predictor of clinical outcome in critically ill children. Nutrition 28:267–270
doi: 10.1016/j.nut.2011.05.015
Ross F, Latham G, Joffe D, Richards M, Geiduschek J, Eisses M, Thompson D, Radman M (2017) Preoperative malnutrition is associated with increased mortality and adverse outcomes after paediatric cardiac surgery. Cardiol Young 27:1716–1725
pubmed: 28625194
pmcid: 5908464
doi: 10.1017/S1047951117001068
van Puffelen E, Hulst JM, Vanhorebeek I, Dulfer K, Van den Berghe G, Verbruggen S, Joosten KFM (2018) Outcomes of delaying parenteral nutrition for 1 week vs initiation within 24 hours among undernourished children in pediatric intensive care: a subanalysis of the PEPaNIC randomized clinical trial. JAMA Netw Open 1:e182668
pubmed: 30646158
pmcid: 6324499
doi: 10.1001/jamanetworkopen.2018.2668
Irving SY, Daly B, Verger J, Typpo KV, Brown AM, Hanlon A, Weiss SL, Fitzgerald JC, Nadkarni VM, Thomas NJ, Srinivasan V, Sepsis Prevalence O, Therapies Study I, Pediatric Acute Lung I, Sepsis Investigators N (2018) The association of nutrition status expressed as body mass index z score with outcomes in children with severe sepsis: a secondary analysis from the Sepsis Prevalence, Outcomes, and Therapies (SPROUT) Study. Crit Care Med 46:e1029–e1039
doi: 10.1097/CCM.0000000000003351
Prince NJ, Brown KL, Mebrahtu TF, Parslow RC, Peters MJ (2014) Weight-for-age distribution and case-mix adjusted outcomes of 14,307 paediatric intensive care admissions. Intensive Care Med 40:1132–1139
pubmed: 25034475
pmcid: 4107282
doi: 10.1007/s00134-014-3381-x
Ravishankar C, Zak V, Williams IA, Bellinger DC, Gaynor JW, Ghanayem NS, Krawczeski CD, Licht DJ, Mahony L, Newburger JW, Pemberton VL, Williams RV, Sananes R, Cook AL, Atz T, Khaikin S, Hsu DT, Pediatric Heart Network I (2013) Association of impaired linear growth and worse neurodevelopmental outcome in infants with single ventricle physiology: a report from the pediatric heart network infant single ventricle trial. J Pediatr 162(250–256):e252
Medoff-Cooper B, Irving SY, Hanlon AL, Golfenshtein N, Radcliffe J, Stallings VA, Marino BS, Ravishankar C (2016) The association among feeding mode, growth, and developmental outcomes in infants with complex congenital heart disease at 6 and 12 months of age. J Pediatr 169(154–159):e151
Knirsch W, Zingg W, Bernet V, Balmer C, Dimitropoulos A, Pretre R, Bauersfeld U, Latal B (2010) Determinants of body weight gain and association with neurodevelopmental outcome in infants operated for congenital heart disease. Interact Cardiovasc Thorac Surg 10:377–382
pubmed: 19959555
doi: 10.1510/icvts.2009.216135
Heye KN, Rousson V, Knirsch W, Beck I, Liamlahi R, Bernet V, Dave H, Latal B, Heart, Brain Research G (2019) Growth and intellectual abilities of six-year-old children with congenital heart disease. J Pediatr 204(24–30):e10
Mehta NM, Corkins MR, Lyman B, Malone A, Goday PS, Carney LN, Monczka JL, Plogsted SW, Schwenk WF, American Society for P, Enteral Nutrition Board of D (2013) Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions. JPEN J Parenter Enteral Nutr 37:460–481
doi: 10.1177/0148607113479972
Koletzko B, Goulet O, Jochum F, Shamir R (2017) Use of parenteral nutrition in the pediatric ICU: should we panic because of PEPaNIC? Curr Opin Clin Nutr Metab Care 20:201–203
pubmed: 28306567
doi: 10.1097/MCO.0000000000000371
Verlinden I, Coppens G, Vanhorebeek I, Guiza F, Derese I, Wouters PJ, Joosten KF, Verbruggen SC, Van den Berghe G (2023) Long-term impact of paediatric critical illness on the difference between epigenetic and chronological age in relation to physical growth. Clin Epigenetics 15:8
pubmed: 36639798
pmcid: 9840263
doi: 10.1186/s13148-023-01424-w
Manning JC, Pinto NP, Rennick JE, Colville G, Curley MAQ (2018) Conceptualizing post intensive care syndrome in children-the PICS-p framework. Pediatr Crit Care Med 19:298–300
pubmed: 29406379
doi: 10.1097/PCC.0000000000001476
Watson RS, Choong K, Colville G, Crow S, Dervan LA, Hopkins RO, Knoester H, Pollack MM, Rennick J, Curley MAQ (2018) Life after critical illness in children-toward an understanding of pediatric post-intensive care syndrome. J Pediatr 198:16–24
pubmed: 29728304
doi: 10.1016/j.jpeds.2017.12.084
Verlinden I, Guiza F, Dulfer K, Van Cleemput H, Wouters PJ, Guerra GG, Joosten KF, Verbruggen SC, Vanhorebeek I, Van den Berghe G (2022) Physical, emotional/behavioral, and neurocognitive developmental outcomes from 2 to 4 years after PICU admission: a secondary analysis of the early versus late parenteral nutrition randomized controlled trial cohort. Pediatr Crit Care Med 23(8):580–592
pubmed: 35522534
pmcid: 9345517
doi: 10.1097/PCC.0000000000002971
Miller TA, Zak V, Shrader P, Ravishankar C, Pemberton VL, Newburger JW, Shillingford AJ, Dagincourt N, Cnota JF, Lambert LM, Sananes R, Richmond ME, Hsu DT, Miller SG, Zyblewski SC, Williams RV, Pediatric Heart Network I (2016) Growth asymmetry, head circumference, and neurodevelopmental outcomes in infants with single ventricles. J Pediatr 168(220–225):e221