Toward Improved Neurodevelopmental Outcomes: The Role of Transfontanel Ultrasound Assessment of Cerebral Blood Flow in Infants Undergoing Cardiac Surgery

Abstract

AS MANY as half of the children undergoing congenital heart surgery in infancy have subsequent neurodevelopmental disabilities.1Wernovsky G. Licht D.J. Neurodevelopmental outcomes in children with congenital heart disease-what can we impact?.Pediatr Crit Care Med. 2016; 17: S232-S242Crossref PubMed Scopus (127) Google Scholar, 2Gaynor J.W. Stopp C. Wypij D. et al.Neurodevelopmental outcomes after cardiac surgery in infancy.Pediatrics. 2015; 135: 816-825Crossref PubMed Scopus (312) Google Scholar, 3Mussatto K.A. Hoffmann R.G. Hoffman G.M. et al.Risk and prevalence of developmental delay in young children with congenital heart disease.Pediatrics. 2014; 133: e570-e577Crossref PubMed Scopus (143) Google Scholar Such disabilities range from mild to severe and include expressive speech and cognitive delays, attention-deficit hyperactivity disorder, motor delay, and impaired executive function. These neurodevelopmental disabilities have a significant impact on the child’s quality of life as well as their families.4Ringle M.L. Wernovsky G. Functional, quality of life, and neurodevelopmental outcomes after congenital cardiac surgery.Semin Perinatol. 2016; 40: 556-570Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar Infants with congenital heart disease (CHD) may have structural brain changes at birth. Preoperative brain magnetic resonance imaging in infants with CHD has detected a 26% incidence of brain abnormalities, which are predominately white matter injury, but also includes cerebral infarcts and hemorrhages.5Rios D.R. Welty S.E. Gunn J.K. et al.Usefulness of routine head ultrasound scans before surgery for congenital heart disease.Pediatrics. 2013; 131: e1765-e1770Crossref Scopus (23) Google Scholar Interestingly when head ultrasounds are performed in these same infants it is able to detect only a 3% incidence of brain injury. However, it is often difficult to obtain brain magnetic resonance imaging in critically ill infants with CHD.5Rios D.R. Welty S.E. Gunn J.K. et al.Usefulness of routine head ultrasound scans before surgery for congenital heart disease.Pediatrics. 2013; 131: e1765-e1770Crossref Scopus (23) Google Scholar In order to minimize further insults to the infant developing brain, multiple cerebral protection strategies during cardiac surgery have been developed. These strategies include monitoring for adequate cerebral blood flow and cerebral oxygenation during the pre- and postoperative periods, as well as during cardiac surgery.6Cheng H.H. Wypij D. Laussen P.C. et al.Cerebral blood flow velocity and neurodevelopmental outcome in infants undergoing surgery for congenital heart disease.Ann Thorac Surg. 2014; 98: 125-132Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar Intraoperative cerebral protection strategies include decreasing cerebral metabolism with moderate hypothermia, minimizing the length of deep hypothermic circulatory arrest, utilizing a pH-stat blood gas management strategy during cooling to deep hypothermic circulatory arrest, keeping the hematocrit higher than 24%, and strict glucose control. Such neuroprotective strategies currently are believed to reduce brain injury and improve neurodevelopmental outcomes.1Wernovsky G. Licht D.J. Neurodevelopmental outcomes in children with congenital heart disease-what can we impact?.Pediatr Crit Care Med. 2016; 17: S232-S242Crossref PubMed Scopus (127) Google Scholar, 7Jonas R.A. Bellinger D.C. Rappaport L.A. et al.Relation of pH strategy and developmental outcome after hypothermic circulatory arrest.J Thorac Cardiovasc Surg. 1993; 106: 362-368Abstract Full Text PDF PubMed Google Scholar Monitoring the brain to ensure adequate blood flow and cerebral oxygenation during cardiopulmonary bypass has progressed extensively over the last 6 decades. Miyazaki and Kato first reported the use of Doppler ultrasound recordings of blood flow velocity in extracranial arteries in 1965.8Miyazaki M. Kato K. Measurement of cerebral blood flow by ultrasonic doppler technique.Jpn Circ J. 1965; 29: 375-382Crossref PubMed Scopus (28) Google Scholar Fifteen years later, Friedrich and colleagues described the use of intraoperative Doppler sonography of brain vessels during neurosurgery.9Friedrich H. Hansel-Friedrich G. Seeger W. [Intraoperative doppler sonography of brain vessels (author's transl)] [in German].Neurochirurgia (Stuttg). 1980; 23: 89-98PubMed Google Scholar In 1982, Aaslid and colleagues reported on the use of noninvasive, transcranial Doppler (TCD) of blood flow velocities in the middle, anterior, and posterior cerebral arteries.10Aaslid R. Markwalder T.M. Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries.J Neurosurg. 1982; 57: 769-774Crossref PubMed Scopus (2325) Google Scholar Soon after this, multiple researchers described the role of TCD to detect cerebral emboli and cerebral blood flow velocities during cardiopulmonary bypass in children. While TCD is not the easiest monitoring modality to use clinically, many cardiac surgical centers currently use TCD.11Deverall P.B. Padayachee T.S. Parsons S. et al.Ultrasound detection of micro-emboli in the middle cerebral artery during cardiopulmonary bypass surgery.Eur J Cardiothorac Surg. 1988; 2: 256-260Crossref PubMed Scopus (42) Google Scholar, 12Van der Linden J. Priddy R. Ekroth R. et al.Cerebral perfusion and metabolism during profound hypothermia in children. A study of middle cerebral artery ultrasonic variables and cerebral extraction of oxygen.J Thorac Cardiovasc Surg. 1991; 102: 103-114Abstract Full Text PDF PubMed Google Scholar, 13Van der Linden J. Wesslen O. et al.Transcranial Doppler-estimated versus thermodilution-estimated cerebral blood flow during cardiac operations. Influence of temperature and arterial carbon dioxide tension.J Thorac Cardiovasc Surg. 1991; 102: 95-102Abstract Full Text PDF PubMed Google Scholar, 14Burrows F.A. Bissonnette B. Cerebral blood flow velocity patterns during cardiac surgery utilizing profound hypothermia with low-flow cardiopulmonary bypass or circulatory arrest in neonates and infants.Can J Anaesth. 1993; 40: 298-307Crossref PubMed Scopus (33) Google Scholar Neonatal brain ultrasonography is an imaging technique initially described in 1976, and again in 1981, that allows interpretation of the anatomical structures within the neonatal cranial vault.15Ovakimian E.S. Oganesian S.S. Vartanian T.V. et al.[Diagnosis of certain intracranial pathological processes in newborn infants by the method of echoencephalography] [in Russian].Pediatriia. 1976; : 23-25PubMed Google Scholar, 16Herbert R. McGrath A. Ultrasonic investigation of the brain in neonates.Radiography. 1981; 47: 187-192PubMed Google Scholar The first few months of life are an ideal time for this analysis as the infant fontanelles are open prior to fusion of the skull bones. The different acoustic impedances of the brain structures allow high-resolution anatomical images to be acquired through the fontanelles.17Huisman T.A. Singhi S. Pinto P.S. Non-invasive imaging of intracranial pediatric vascular lesions.Childs Nerv Syst. 2010; 26: 1275-1295Crossref PubMed Scopus (21) Google Scholar In addition, Doppler ultrasound spectral analysis, usually along a branch of the circle of Willis, allows anterior cerebral artery (ACA) flow signals to be measured, and the basilar artery (BA) can be analyzed to measure cerebral blood flow in the vertebrobasilar system. These arterial flow patterns allow quantification of peak systolic velocity (PSV) and maximal end-diastolic velocity (EDV). The resistive index (RI) can be calculated using these measurements from the formula RI = (PSV – EDV/PSV). For full-term neonates, the normal RI is 0.65 to 0.75, while premature infants have a higher RI in the range 0.77 to 0.8.17Huisman T.A. Singhi S. Pinto P.S. Non-invasive imaging of intracranial pediatric vascular lesions.Childs Nerv Syst. 2010; 26: 1275-1295Crossref PubMed Scopus (21) Google Scholar, 18Deeg K.H. Rupprecht T. Pulsed Doppler sonographic measurement of normal values for the flow velocities in the intracranial arteries of healthy newborns.Pediatr Radiol. 1989; 19: 71-78Crossref PubMed Scopus (61) Google Scholar, 19Mires G.J. Patel N.B. Forsyth J.S. et al.Neonatal cerebral Doppler flow velocity waveforms in the uncomplicated pre-term infant: Reference values.Early Hum Dev. 1994; 36: 205-212Crossref PubMed Scopus (8) Google Scholar A decrease in RI is seen in brain edema. An increase in EDV may be seen during a loss of cerebral autoregulation or as a compensatory response to hypoperfusion or hypoxia. An elevated RI usually is due to a decrease in EDV related to increased intracranial pressure.17Huisman T.A. Singhi S. Pinto P.S. Non-invasive imaging of intracranial pediatric vascular lesions.Childs Nerv Syst. 2010; 26: 1275-1295Crossref PubMed Scopus (21) Google Scholar, 20Daneman A. Epelman M. Blaser S. et al.Imaging of the brain in full-term neonates: Does sonography still play a role?.Pediatr Radiol. 2006; 36: 636-646Crossref PubMed Scopus (77) Google Scholar End-diastolic block is diagnosed when end-diastolic blood flow is found to be absent from the cranial Doppler waveforms for at least 20 consecutive cardiac cycles in the ACA or BA.21Julkunen M. Parviainen T. Janas M. et al.End-diastolic block in cerebral circulation may predict intraventricular hemorrhage in hypotensive extremely-low-birth-weight infants.Ultrasound Med Biol. 2008; 34: 538-545Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar The occurrence of end-diastolic block in either the ACA or BA, a mean arterial pressure <30 mmHg, and a patent ductus arteriosus (PDA) appears to correlate with the development of an intraventricular hemorrhage in infants with a birthweight <1,000 gm.21Julkunen M. Parviainen T. Janas M. et al.End-diastolic block in cerebral circulation may predict intraventricular hemorrhage in hypotensive extremely-low-birth-weight infants.Ultrasound Med Biol. 2008; 34: 538-545Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar The “Ductal steal phenomenon” is often used in this context to describe a sharp decrease in diastolic flow velocity and an increase in pulse amplitude in the ACA in the presence of a large unrestricted PDA.22Perlman J.M. Hill A. Volpe J.J. The effect of patent ductus arteriosus on flow velocity in the anterior cerebral arteries: Ductal steal in the premature newborn infant.J Pediatr. 1981; 99: 767-771Abstract Full Text PDF PubMed Scopus (181) Google Scholar In this issue of the Journal of Cardiothoracic and Vascular Anesthesia, Kim and colleagues describe the role of transfontanel ultrasound measurements of cerebral arterial blood flow velocity as a noninvasive neuromonitoring modality in 10 patients (median age 24.5 days [range 4-74 days]; median weight, 3.5 kg [range 2.9-4.8 kg]) undergoing modified Blalock-Taussig shunt (MBTS) surgery.23Kim E-H Lee J-H Song I-K et al.Potential role of transfontanelle ultrasound for infants undergoing modified Blalock-Taussig shunt.J Cardiothorac Vasc Anesth. 2018; 32: 1648-1654Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar This retrospective study follows the introduction of the routine use of transfontanel cerebral blood flow velocity monitoring during cardiac surgery at their institution. They explain how their observations of cerebral blood flow velocities during MBTS surgery led to the detection of the “ductal steal phenomenon” prior to surgical ligation of the ductus arteriosus, but also discovered the oversizing of the MBTS in one infant in their series.23Kim E-H Lee J-H Song I-K et al.Potential role of transfontanelle ultrasound for infants undergoing modified Blalock-Taussig shunt.J Cardiothorac Vasc Anesth. 2018; 32: 1648-1654Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar This work by Kim and colleagues is very interesting because it describes cerebral blood flow velocity related to the presence of a surgically made shunt and raises the possibility of guiding the size of MBTS in order to prevent the steal of cerebral blood flow. However, this transfontanel Doppler technique requires significant training and experience to achieve accurate and reliable results. De Waal reminds us that ultrasound derived measurement of blood flow velocities in newborn infants, even of the left ventricular outflow tract through the chest, may be very variable depending on multiple factors. These factors include: methodology of vessel diameter determination (M mode versus 2D, leading edge versus trailing edge technique), Doppler method (continuous Doppler versus pulse-wave Doppler), and ultrasound probe location (suprasternal versus subcostal or apical).24de Waal K.A. The methodology of Doppler-derived central blood flow measurements in newborn infants.Int J Pediatr. 2012; 2012: 680162Crossref PubMed Google Scholar Kim and colleagues conclude that this noninvasive transfontanel technique warrants further study as it may be a very helpful adjunct in the neuromonitoring of infants undergoing cardiac surgery. Specifically, this technique potentially could measure the “cerebral blood flow steal phenomenon” and prevent too large a MBTS being placed inadvertently. All of the advances in the perioperative and surgical management of infants with CHD over the last decades have resulted in improved long-term survival and is a remarkable success story. However, improving neurodevelopmental outcomes in children undergoing congenital heart surgery during infancy remains one of the most important clinical goals of the multidisciplinary care team. Monitoring the brain during cardiac surgery remains a key component to the anticipated improved neurodevelopmental outcomes in these children. Kim and colleagues have helped us take another small step toward this goal.