Postoperative Cerebral Oxygen Saturation in Children After Congenital Cardiac Surgery and Long-Term Total Intelligence Quotient: A Prospective Observational Study

Giorgia Carra, Marine Flechet, An Jacobs, Sören Verstraete, Dirk Vlasselaers, Lars Desmet, Hanna Van Cleemput, Pieter Wouters, Ilse Vanhorebeek, Greet Van den Berghe, Fabian Güiza, Geert Meyfroidt, Giorgia Carra, Marine Flechet, An Jacobs, Sören Verstraete, Dirk Vlasselaers, Lars Desmet, Hanna Van Cleemput, Pieter Wouters, Ilse Vanhorebeek, Greet Van den Berghe, Fabian Güiza, Geert Meyfroidt

Abstract

Objectives: During the early postoperative period, children with congenital heart disease can suffer from inadequate cerebral perfusion, with possible long-term neurocognitive consequences. Cerebral tissue oxygen saturation can be monitored noninvasively with near-infrared spectroscopy. In this prospective study, we hypothesized that reduced cerebral tissue oxygen saturation and increased intensity and duration of desaturation (defined as cerebral tissue oxygen saturation < 65%) during the early postoperative period, independently increase the probability of reduced total intelligence quotient, 2 years after admission to a PICU.

Design: Single-center, prospective study, performed between 2012 and 2015.

Setting: The PICU of the University Hospitals Leuven, Belgium.

Patients: The study included pediatric patients after surgery for congenital heart disease admitted to the PICU.

Interventions: None.

Measurements and main results: Postoperative cerebral perfusion was characterized with the mean cerebral tissue oxygen saturation and dose of desaturation of the first 12 and 24 hours of cerebral tissue oxygen saturation monitoring. The independent association of postoperative mean cerebral tissue oxygen saturation and dose of desaturation with total intelligence quotient at 2-year follow-up was evaluated with a Bayesian linear regression model adjusted for known confounders. According to a noninformative prior, reduced mean cerebral tissue oxygen saturation during the first 12 hours of monitoring results in a loss of intelligence quotient points at 2 years, with a 90% probability (posterior β estimates [80% credible interval], 0.23 [0.04-0.41]). Similarly, increased dose of cerebral tissue oxygen saturation desaturation would result in a loss of intelligence quotient points at 2 years with a 90% probability (posterior β estimates [80% credible interval], -0.009 [-0.016 to -0.001]).

Conclusions: Increased dose of cerebral tissue oxygen saturation desaturation and reduced mean cerebral tissue oxygen saturation during the early postoperative period independently increase the probability of having a lower total intelligence quotient, 2 years after PICU admission.

Trial registration: ClinicalTrials.gov NCT01706497.

Conflict of interest statement

Ms. Carra receives funding from the Research Foundation, Flanders (FWO) as a PhD fellow (fellowship number: 1S28120N). Dr. Meyfroidt is supported by the Research Foundation, Flanders (FWO) as senior clinical investigator (1843118N). Drs. Güiza and Meyfroidt receive project funding from the KU Leuven (C2 project [C24/17/072]: a Neuromonitor for the 21st century). Drs. Flechet and Verstraete received funding from the Research Foundation, Flanders (FWO) as PhD fellows (fellowship numbers: 11Y1118N and 11V9215N, respectively). Ms. Carra and Dr. Meyfroidt received a PhD fellowship from the FWO (Belgium). The remaining authors have disclosed that they do not have any potential conflicts of interest.

Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the Society of Critical Care Medicine and Wolters Kluwer Health, Inc.

Figures

Figure 1.
Figure 1.
Sequences of regional cerebral tissue oxygen saturation (Scto2) recordings, first 12 hr of monitoring time. Signal A desaturation dose: 0%·min, mean Scto2: 74%. Signal B desaturation dose: 917 %·min; mean Scto2: 57%. For signal B, the desaturation dose below 65% (unit of measurement: %·min) is represented by the dark-gray area between the signal and the gray dashed line, which indicates the 65% desaturation threshold. According to the enthusiastic prior, there is an 80% probability that the dose of desaturation of signal B results in a loss of 4–15 IQ points as compared with signal A. Similarly, there is an 80% probability that the mean Scto2 of signal B results in 2.8–7.4 IQ points lower total IQ than signal A 2-yr after pediatric intensive care medicine admission.
Figure 2.
Figure 2.
Flow diagram for study participants inclusion. NIRS = near-infrared spectroscopy.
Figure 3.
Figure 3.
Comparison between the β priors and β posteriors probability distribution of the skeptical, neutral, and enthusiastic priors of the multivariable Bayesian model on the relation between mean regional cerebral tissue oxygen saturation (Scto2) and total IQ. Only the distributions of the β estimate of the mean Scto2 (first 12 hr of monitoring time) are shown.

References

    1. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol. 2002; 39:1890–1900
    1. Glass TJA, Seed M, Chau V: Chapter 15 - Congenital Heart Disease: An Important Cause of Brain Injury and Dysmaturation. Third Edition. Elsevier Inc.; 2019
    1. Galli KK, Zimmerman RA, Jarvik GP, et al. . Periventricular leukomalacia is common after neonatal cardiac surgery. J Thorac Cardiovasc Surg. 2004; 127:692–704
    1. Bellinger DC, Wypij D, Kuban KC, et al. . Developmental and neurological status of children at 4 years of age after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. Circulation. 1999; 100:526–532
    1. Majnemer A, Limperopoulos C. Developmental progress of children with congenital heart defects requiring open heart surgery. Semin Pediatr Neurol. 1999; 6:12–19
    1. Gaynor JW, Stopp C, Wypij D, et al. ; International Cardiac Collaborative on Neurodevelopment (ICCON) Investigators. Neurodevelopmental outcomes after cardiac surgery in infancy. Pediatrics. 2015; 135:816–825
    1. Kinney HC, Panigrahy A, Newburger JW, et al. . Hypoxic-ischemic brain injury in infants with congenital heart disease dying after cardiac surgery. Acta Neuropathol. 2005; 110:563–578
    1. Wernovsky G, Licht DJ. Neurodevelopmental outcomes in children with congenital heart disease-what can we impact? Pediatr Crit Care Med. 2016; 17:S232–S242
    1. Ghanayem NS, Wernovsky G, Hoffman GM. Near-infrared spectroscopy as a hemodynamic monitor in critical illness. Pediatr Crit Care Med. 2011; 12:S27–S32
    1. Zulueta JL, Vida VL, Perisinotto E, et al. . Role of intraoperative regional oxygen saturation using near infrared spectroscopy in the prediction of low output syndrome after pediatric heart surgery. J Card Surg. 2013; 28:446–452
    1. Fenton KN, Freeman K, Glogowski K, et al. . The significance of baseline cerebral oxygen saturation in children undergoing congenital heart surgery. Am J Surg. 2005; 190:260–263
    1. Dent CL, Spaeth JP, Jones BV, et al. . Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion. J Thorac Cardiovasc Surg. 2005; 130:1523–1530
    1. Flechet M, Güiza F, Vlasselaers D, et al. . Near-infrared cerebral oximetry to predict outcome after pediatric cardiac surgery: A prospective observational study. Pediatr Crit Care Med. 2018; 19:433–441
    1. Zaleski KL, Kussman BD. Near-infrared spectroscopy in pediatric congenital heart disease. J Cardiothorac Vasc Anesth. 2020; 34:489–500
    1. Vida VL, Tessari C, Cristante A, et al. . The role of regional oxygen saturation using near-infrared spectroscopy and blood lactate levels as early predictors of outcome after pediatric cardiac surgery. Can J Cardiol. 2016; 32:970–977
    1. Slater JP, Guarino T, Stack J, et al. . Cerebral oxygen desaturation predicts cognitive decline and longer hospital stay after cardiac surgery. Ann Thorac Surg. 2009; 87:36–44
    1. Flechet M, Güiza F, Scharlaeken I, et al. . Near-infrared-based cerebral oximetry for prediction of severe acute kidney injury in critically ill children after cardiac surgery. Crit Care Explor. 2019; 1:e0063.
    1. Verstraete S, Verbruggen SC, Hordijk JA, et al. . 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. 2019; 7:141–153
    1. Hendriksen J, Hurks P: WPPSI-III-NL | Wechsler Preschool and Primary Scale of Intelligence. 2010
    1. Wechsler D: WISC-III-NL | Wechsler Intelligence Scale for Children-III. Amsterdam, The Netherlands, 2005
    1. Miatton M, De Wolf D, François K, et al. . Neurocognitive consequences of surgically corrected congenital heart defects: A review. Neuropsychol Rev. 2006; 16:65–85
    1. Palmer SL, Hassall T, Evankovich K, et al. . Neurocognitive outcome 12 months following cerebellar mutism syndrome in pediatric patients with medulloblastoma. Neuro Oncol. 2010; 12:1311–1317
    1. Virtanen R, Korhonen T, Fagerholm J, et al. . Neurocognitive sequelae of scaphocephaly. Pediatrics. 1999; 103:791–795
    1. van der Sluijs Veer L, Kempers MJ, Wiedijk BM, et al. . Evaluation of cognitive and motor development in toddlers with congenital hypothyroidism diagnosed by neonatal screening. J Dev Behav Pediatr. 2012; 33:633–640
    1. Armstrong-Wells J, Bernard TJ, Boada R, et al. . Neurocognitive outcomes following neonatal encephalopathy. NeuroRehabilitation. 2010; 26:27–33
    1. Hövels-Gürich HH, Seghaye MC, Däbritz S, et al. . Cognitive and motor development in preschool and school-aged children after neonatal arterial switch operation. J Thorac Cardiovasc Surg. 1997; 114:578–585
    1. Limperopoulos C, Majnemer A, Shevell MI, et al. . Predictors of developmental disabilities after open heart surgery in young children with congenital heart defects. J Pediatr. 2002; 141:51–58
    1. Oster ME, Lee KA, Honein MA, et al. . Temporal trends in survival among infants with critical congenital heart defects. Pediatrics. 2013; 131:e1502–e1508
    1. Kussman BD, Wypij D, Laussen PC, et al. . Relationship of intraoperative cerebral oxygen saturation to neurodevelopmental outcome and brain magnetic resonance imaging at 1 year of age in infants undergoing biventricular repair. Circulation. 2010; 122:245–254
    1. Spaeder MC, Klugman D, Skurow-Todd K, et al. . Perioperative near-infrared spectroscopy monitoring in neonates with congenital heart disease: Relationship of cerebral tissue oxygenation index variability with neurodevelopmental outcome. Pediatr Crit Care Med. 2017; 18:213–218
    1. Hoffman GM, Ghanayem NS, Scott JP, et al. . Postoperative cerebral and somatic near-infrared spectroscopy saturations and outcome in hypoplastic left heart syndrome. Ann Thorac Surg. 2017; 103:1527–1535
    1. McNeill S, Gatenby JC, McElroy S, et al. . Normal cerebral, renal and abdominal regional oxygen saturations using near-infrared spectroscopy in preterm infants. J Perinatol. 2011; 31:51–57
    1. Dix LML, van Bel F, Lemmers PMA. Monitoring cerebral oxygenation in neonates: An update. Front Pediatr. 2018; 5:1–9
    1. Neshat Vahid S, Panisello JM. The state of affairs of neurologic monitoring by near-infrared spectroscopy in pediatric cardiac critical care. Curr Opin Pediatr. 2014; 26:299–303

Source: PubMed

3
Subskrybuj