Brain volume and metabolism in fetuses with congenital heart disease: Evaluation with quantitative magnetic resonance imaging and spectroscopy

Circulation

Volumn 121, Issue 1, 2010, Pages 26-33

  Limperopoulos, Catherine ^a,b   Tworetzky, Wayne ^c   McElhinney, Doff B ^c   Newburger, Jane W ^c   Brown, David W ^c   Robertson, Richard L ^c   Guizard, Nicolas ^a   McGrath, Ellen ^c   Geva, Judith ^c   Annese, David ^c   Dunbar Masterson, Carolyn ^c   Trainor, Bethany ^c   Laussen, Peter C ^d   Du Plessis, Adré J ^b  

^a MCGILL UNIVERSITY   (Canada)

^b Fetal Neonatal Neurology Research Group   (United States)

^c Department of Cardiology and Pediatrics ^*

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Brain; Congenital; Fetal; Magnetic resonance imaging; Pediatrics

Indexed keywords

CHOLINE; LACTIC ACID; N ACETYLASPARTIC ACID;

AORTA ARCH; ARTERY BLOOD FLOW; ARTICLE; BRAIN FUNCTION; BRAIN METABOLISM; BRAIN SIZE; CEREBROSPINAL FLUID; CONGENITAL HEART DISEASE; CONTROLLED STUDY; FEMALE; FETUS; FETUS ELECTROCARDIOGRAPHY; GESTATIONAL AGE; HUMAN; MAJOR CLINICAL STUDY; MALE; MORBIDITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; THIRD TRIMESTER PREGNANCY;

ASPARTIC ACID; BRAIN; CHOLINE; FEMALE; GESTATIONAL AGE; HEART DEFECTS, CONGENITAL; HUMANS; IMAGING, THREE-DIMENSIONAL; LACTIC ACID; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; PREGNANCY; PRENATAL DIAGNOSIS; PROSPECTIVE STUDIES; PROTONS;

EID: 74549172520     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.865568     Document Type: Article

References (42)

1. Dittrich H, Buhrer C, Grimmer I, Dittrich S, Abdul-Khaliq H, Lange PE. Neurodevelopment at 1 year of age in infants with congenital heart disease. Heart. 2003;89:436-441.
2. Tabbutt S, Nord AS, Jarvik GP, Bernbaum J, Wernovsky G, Gerdes M, Zackai E, Clancy RR, Nicolson SC, Spray TL, Gaynor JW. Neurodevel-opmental outcomes after staged palliation for hypoplastic left heart syndrome. Pediatrics. 2008;121:476-483.
3. Massaro AN, El-Dib M, Glass P, Aly H. Factors associated with adverse neurodevelopmental outcomes in infants with congenital heart disease. Brain Dev. 2008;30:437-446.
4. Ballweg JA, Wernovsky G, Gaynor JW. Neurodevelopmental outcomes following congenital heart surgery. Pediatr Cardiol. 2007;28:126-133.
5. Newburger JW, Jonas RA, Wernovsky G, Wypij D, Hickey PR, Kuban KCK, Farrell DM, Holmes GL, Helmers SL, Constantinou J, Carrazana E, Barlow JK, Walsh AZ, Lucius KC, Share JC, Wessel DL, Hanley FL, Mayer JE, Castaneda AR, Ware JH. A comparison of the perioperative neurologic effects of hypothermic circulatory arrest versus low-flow cardiopulmonary bypass in infant heart surgery. N Engl J Med. 1993; 329:1057-1064.
6. Jonas RA, Wypij D, Roth SJ, Bellinger DC, Visconti KJ, du Plessis AJ, Goodkin H, Laussen PC, Farrell DM, Bartlett J, McGrath E, Rappaport LJ, Bacha EA, Forbess JM, del Nido PJ, Mayer JE Jr, Newburger JW. The influence of hemodilution on outcome after hypothermic cardiopul-monary bypass: results of a randomized trial in infants. J Thorac Car-diovasc Surg. 2003;126:1765-1774.
7. Newburger JW, Jonas RA, Soul J, Kussman BD, Bellinger DC, Laussen PC, Robertson R, Mayer JE Jr, del Nido PJ, Bacha EA, Forbess JM, Pigula F, Roth SJ, Visconti KJ, du Plessis AJ, Farrell DM, McGrath E, Rappaport LA, Wypij D. Randomized trial of hematocrit 25% versus 35% during hypothermic cardiopulmonary bypass in infant heart surgery. J Thorac Cardiovasc Surg. 2008;135:347-354.
8. Clancy RR, McGaurn SA, Goin JE, Hirtz DG, Norwood WI, Gaynor JW, Jacobs ML, Wernovsky G, Mahle WT, Murphy JD, Nicolson SC, Steven JM, Spray TL. Allopurinol neurocardiac protection trial in infants undergoing heart surgery using deep hypothermic circulatory arrest. Pediatrics. 2001;108:61-70.
9. Limperopoulos C, Majnemer A, Rosenblatt B, Shevell M, Rohlicek C, Tchervenkov C. Multimodality evoked potential findings in infants with congenital heart defects. J Child Neurol. 1999;14:702-707.
10. Limperopoulos C, Majnemer A, Shevell MI, Rosenblatt B, Rohlicek C, Tchervenkov C. Neurodevelopmental status of newborns and infants with congenital heart defects before and after open heart surgery. J Pediatr. 2000;137:638-645.
11. Limperopoulos C, Majnemer A, Rosenblatt B, Shevell MI, Rohlicek C, Tchervenkov C, Gottesman R. Association between electroencephalo-graphic findings and neurologic status in infants with congenital heart defects. J Child Neurol. 2001;16:471-476.
12. Licht DJ, Wang J, Silvestre DW, Nicolson SC, Montenegro LM, Wer-novsky G, Tabbutt S, Durning SM, Shera DM, Gaynor JW, Spray TL, Clancy RR, Zimmerman RA, Detre JA. Preoperative cerebral blood flow is diminished in neonates with severe congenital heart defects. J Thorac Cardiovasc Surg. 2004;128:841-849.
13. Te Pas AB, van Wezel-Meijler G, Bokenkamp-Gramann R, Walther FJ. Preoperative cranial ultrasound findings in infants with major congenital heart disease. Acta Paediatr. 2005;94:1597-1603.
14. Mahle WT, Tavani F, Zimmerman RA, Nicolson SC, Galli KK, Gaynor JW, Clancy RR, Montenegro LM, Spray TL, Chiavacci RM, Wernovsky G, Kurth CD. An MRI study of neurological injury before and after congenital heart surgery. Circulation. 2002;106:I109-I114.
15. Miller SP, McQuillen PS, Hamrick S, Xu D, Glidden DV, Charlton N, Karl T, Azakie A, Ferriero DM, Barkovich AJ, Vigneron DB. Abnormal brain development in newborns with congenital heart disease. N Engl J Med. 2007;357:1928-1938.
16. Hinton RB, Andelfinger G, Sekar P, Hinton AC, Gendron RL, Mich-elfelder EC, Robitaille Y, Benson DW. Prenatal head growth and white matter injury in hypoplastic left heart syndrome. Pediatr Res. 2008;64: 364-369.
17. Licht DJ, Shera DM, Clancy RR, Wernovsky G, Montenegro LM, Nicolson SC, Zimmerman RA, Spray TL, Gaynor JW, Vossough A. Brain maturation is delayed in infants with complex congenital heart defects. J Thorac Cardiovasc Surg. 2009;137:529-536.
18. Limperopoulos C, Majnemer A, Shevell MI, Rohlicek C, Rosenblatt B, Tchervenkov C, Darwish HZ. Predictors of developmental disabilities after open heart surgery in young children with congenital heart defects. J Pediatr. 2002;141:51-58.
19. Majnemer A, Limperopoulos C, Shevell M, Rosenblatt B, Rohlicek C, Tchervenkov C. Long-term neuromotor outcome at school entry of infants with congenital heart defects requiring open-heart surgery. J Pediatr. 2006;148:72-77.
20. Donofrio MT, Bremer YA, Schieken RM, Gennings C, Morton LD, Eidem BW, Cetta F, Falkensammer CB, Huhta JC, Kleinman CS. Auto-regulation of cerebral blood flow in fetuses with congenital heart disease: the brain sparing effect. Pediatr Cardiol. 2003;24:436-443.
21. Kaltman JR, Di H, Tian Z, Rychik J. Impact of congenital heart disease on cerebrovascular blood flow dynamics in the fetus. Ultrasound Obstet Gynecol. 2005;25:32-36.
22. Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight: the value of femur length in addition to head and abdomen measurements. Radiology. 1984;150:535-540.
23. Doubilet PM, Benson CB, Nadel AS, Ringer SA. Improved birth weight table for neonates developed from gestations dated by early ultra-sonography. J Ultrasound Med. 1997;16:241-249.
24. Girard N, Gouny SC, Viola A, Le Fur Y, Viout P, Chaumoitre K, D'Ercole C, Gire C, Figarella-Branger D, Cozzone PJ. Assessment of normal fetal brain maturation in utero by proton magnetic resonance spectroscopy. Magn Reson Med. 2006;56:768-775.
25. Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging. 1998;17:87-97.
26. Guizard N, Lepag C, Fonov V, Hakyemez H, Evans A, Limperopoulos C. Development of a fetal brain atlas from multi-axial MR acquisitions. In: Proceedings of the 16th Scientific Meeting, International Society for Magnetic Resonance in Medicine; May 3-9, 2008; Toronto, Ontario, Canada. Abstract 672.
27. Kok RD, van den Berg PP, van den Bergh AJ, Nijland R, Heerschap A. Maturation of the human fetal brain as observed by 1H MR spectroscopy. Magn Reson Med. 2002;48:611-616.
28. Glauser T, Rorke L, Weinberg P, Clancy R. Congenital brain anomalies associated with the hypoplastic left heart syndrome. Pediatrics. 1990;85: 984-990. (Pubitemid 20184718)
29. Andelfinger G. Genetic factors in congenital heart malformation. Clin Genet. 2008;73:516-527.
30. Petit CJ, Rome JJ, Wernovsky G, Mason SE, Shera DM, Nicolson SC, Montenegro LM, Tabbutt S, Zimmerman RA, Licht DJ. Preoperative brain injury in transposition of the great arteries is associated with oxygenation and time to surgery, not balloon atrial septostomy. Circulation. 2009;119: 709-716.
31. Brody BA, Kinney HC, Kloman AS, Gilles FH. Sequence of central nervous system myelination in human infancy, I: an autopsy study of myelination. J Neuropathol Exp Neurol. 1987;46:283-301.
32. Huppi PS, Warfield S, Kikinis R, Barnes PD, Zientara GP, Jolesz FA, Tsuji MK, Volpe JJ. Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol. 1998;43: 224-235.
33. Edelstone DI, Rudolph AM. Preferential streaming of ductus venosus blood to the brain and heart in fetal lambs. Am J Physiol. 1979;237: 724-729.
34. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, Katz KH, Westerveld M, Sparrow S, Anderson AW, Duncan CC, Makuch RW, Gore JC, Ment LR. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA. 2000;284: 1939-1947.
35. Tolsa CB, Zimine S, Warfield SK, Freschi M, Sancho Rossignol A, Lazeyras F, Hanquinet S, Pfizenmaier M, Huppi PS. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res. 2004;56:132-138.
36. Bhakoo KK, Pearce D. In vitro expression of N-acetyl aspartate by oligodendrocytes: implications for proton magnetic resonance spec-troscopy signal in vivo. J Neurochem. 2000;74:254-262.
37. Demougeot C, Garnier P, Mossiat C, Bertrand N, Giroud M, Beley A, Marie C. N-Acetylaspartate, a marker of both cellular dysfunction and neuronal loss: its relevance to studies of acute brain injury. J Neurochem. 2001;77:408-415.
38. Azpurua H, Alvarado A, Mayobre F, Salom T, Copel JA, Guevara-Zuloaga F. Metabolic assessment of the brain using proton magnetic resonance spectroscopy in a growth-restricted human fetus: case report. Am J Perinatol. 2008;25:305-309.
39. Wolfberg AJ, Robinson JN, Mulkern R, Rybicki F, Du Plessis AJ. Identification of fetal cerebral lactate using magnetic resonance spec-troscopy. Am J Obstet Gynecol. 2007;196:e9-e11.
40. Barkovich AJ, Baranski K, Vigneron D, Partridge JC, Hallam DK, Hajnal BL, Ferriero DM. Proton MR spectroscopy for the evaluation of brain injury in asphyxiated, term neonates. AJNR Am J Neuroradiol. 1999;20: 1399-1405.
41. Girard N, Fogliarini C, Viola A, Confort-Gouny S, Fur YL, Viout P, Chapon F, Levrier O, Cozzone P. MRS of normal and impaired fetal brain development. Eur J Radiol. 2006;57:217-225.
42. Jiang S, Xue H, Glover A, Rutherford M, Rueckert D, Hajnal JV. MRI of moving subjects using multislice snapshot images with volume reconstruction (SVR): application to fetal, neonatal, and adult brain studies. IEEE Trans Med Imaging. 2007;26:967-980.