Download PDF
CC BY-NC-ND 4.0 · AJP Rep 2017; 07(01): e17-e27
DOI: 10.1055/s-0036-1597934
Case Report
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Synchronous Aberrant Cerebellar and Opercular Development in Fetuses and Neonates with Congenital Heart Disease: Correlation with Early Communicative Neurodevelopmental Outcomes, Initial Experience

A. Wong
1   New York Medical College, Valhalla, New York
,
T. Chavez
2   Division of Neonatology, University Southern California, Children's Hospital Los Angeles Center for Fetal and Neonatal Medicine, Los Angeles, California
,
S. O'Neil
3   Division of Neurology, University Southern California, Children's Hospital Los Angeles, Los Angeles, California
,
J. Votava-Smith
4   Division of Cardiology, University Southern California, Children's Hospital Los Angeles, Los Angeles, California
,
D. Miller
7   Division of Obstetrics/Gynecology, University Southern California, Children's Hospital Los Angeles Center for Fetal and Neonatal Medicine, Los Angeles, California
,
S. delCastillo
5   Division of Anesthesiology Critical Care Medicine, University Southern California, Children's Hospital Los Angeles, Los Angeles, California
,
A. Panigrahy
6   Department of Radiology, University of Pittsburgh, Children's Hospital of Pittsburgh of UPMC, Pittsburgh, Pennsylvania
,
L. Paquette
2   Division of Neonatology, University Southern California, Children's Hospital Los Angeles Center for Fetal and Neonatal Medicine, Los Angeles, California
› Author Affiliations
Further Information

Publication History

22 September 2016

03 November 2016

Publication Date:
13 February 2017 (online)

   Permissions and Reprints

Abstract

Patients with congenital heart disease (CHD) demonstrate multidomain cognitive delays. Cingulo-opercular and cerebellar brain networks are critical to language functions. This is a description of our initial experience aiming to identify an anatomic correlate for CHD patients with expressive language delays. Fetal CHD patients, prospectively enrolled, underwent serial fetal (1.5T), postnatal pre- and postoperative (3T) MRI. Non-CHD patients were enrolled retrospectively from the same epoch. Comparable fetal and neonatal T2 contrast was used for manual linear cross-sectional measurement. Multivariable analysis was used for adjustments and curve fitting. Neurodevelopment was assessed with Battelle Developmental Inventory, 2nd ed. between 9 and 36 months of age. This interim analysis included patients from our longitudinal CHD study who had fetal, postnatal imaging and neurodevelopmental data—yielding a total of 62 mothers (11 CHD fetuses and 51 non-CHD fetuses). Altered brain trajectories were seen in selected cerebellar and opercular measurements in CHD patients compared with the non-CHD group. Smaller inferior cerebellar vermis measurements were associated with multiple communication-related abnormalities. Altered early structural development of the cerebellum and operculum is present in patients with CHD, which correlates with specific neurodevelopmental abnormalities.

Keywords

congenital heart disease - fetus - neonate - brain growth - neurodevelopment - communication
 

  • References

  • 1 Mahle WT, Clancy RR, Moss EM, Gerdes M, Jobes DR, Wernovsky G. Neurodevelopmental outcome and lifestyle assessment in school-aged and adolescent children with hypoplastic left heart syndrome. Pediatrics 2000; 105 (05) 1082-1089
    CrossrefPubMedGoogle Scholar
  • 2 Marino BS, Lipkin PH, Newburger JW. , et al; American Heart Association Congenital Heart Defects Committee, Council on Cardiovascular Disease in the Young, Council on Cardiovascular Nursing, and Stroke Council. Neurodevelopmental outcomes in children with congenital heart disease: evaluation and management: a scientific statement from the American Heart Association. Circulation 2012; 126 (09) 1143-1172
    CrossrefPubMedGoogle Scholar
  • 3 Licht DJ, Shera DM, Clancy RR. , et al. Brain maturation is delayed in infants with complex congenital heart defects. J Thorac Cardiovasc Surg 2009; 137 (03) 529-536 , discussion 536–537
    CrossrefPubMedGoogle Scholar
  • 4 Limperopoulos C, Tworetzky W, McElhinney DB. , et al. Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation 2010; 121 (01) 26-33
    CrossrefPubMedGoogle Scholar
  • 5 Bellinger DC, Wypij D, duPlessis AJ. , et al. Neurodevelopmental status at eight years in children with dextro-transposition of the great arteries: the Boston Circulatory Arrest Trial. J Thorac Cardiovasc Surg 2003; 126 (05) 1385-1396
    CrossrefPubMedGoogle Scholar
  • 6 Hövels-Gürich HH, Konrad K, Skorzenski D. , et al. Long-term neurodevelopmental outcome and exercise capacity after corrective surgery for tetralogy of Fallot or ventricular septal defect in infancy. Ann Thorac Surg 2006; 81 (03) 958-966
    CrossrefPubMedGoogle Scholar
  • 7 Murdoch BE. The cerebellum and language: historical perspective and review. Cortex 2010; 46 (07) 858-868
    CrossrefPubMedGoogle Scholar
  • 8 Leiner HC, Leiner AL, Dow RS. Reappraising the cerebellum: what does the hindbrain contribute to the forebrain?. Behav Neurosci 1989; 103 (05) 998-1008
    CrossrefPubMedGoogle Scholar
  • 9 Desmond JE, Gabrieli JDE, Glover GH. Dissociation of frontal and cerebellar activity in a cognitive task: evidence for a distinction between selection and search. Neuroimage 1998; 7 (4 Pt 1): 368-376
    CrossrefPubMedGoogle Scholar
  • 10 Tamburrini G, Frassanito P, Chieffo D, Massimi L, Caldarelli M, Di Rocco C. Cerebellar mutism. Childs Nerv Syst 2015; 31 (10) 1841-1851
    CrossrefPubMedGoogle Scholar
  • 11 Allen G, McColl R, Barnard H, Ringe WK, Fleckenstein J, Cullum CM. Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. Neuroimage 2005; 28 (01) 39-48
    CrossrefPubMedGoogle Scholar
  • 12 Wise RJ, Greene J, Büchel C, Scott SK. Brain regions involved in articulation. Lancet 1999; 353 (9158): 1057-1061
    CrossrefPubMedGoogle Scholar
  • 13 Baillieux H, De Smet HJ, Paquier PF, De Deyn PP, Mariën P. Cerebellar neurocognition: insights into the bottom of the brain. Clin Neurol Neurosurg 2008; 110 (08) 763-773
    CrossrefPubMedGoogle Scholar
  • 14 Chen CY, Zimmerman RA, Faro S. , et al. MR of the cerebral operculum: topographic identification and measurement of interopercular distances in healthy infants and children. AJNR Am J Neuroradiol 1995; 16 (08) 1677-1687
    PubMedGoogle Scholar
  • 15 Larroche JC. Developmental pathology of the neonate. In: Development of the Central Nervous System. Amsterdam,. The Netherlands: Excerpta Medica; 1977: 319-327
    Google Scholar
  • 16 Tatum WO, Coker SB, Ghobrial M, Abd-Allah S. The open opercular sign: diagnosis and significance. Ann Neurol 1989; 25 (02) 196-199
    CrossrefPubMedGoogle Scholar
  • 17 Chen CY, Zimmerman RA, Faro S. , et al. MR of the cerebral operculum: abnormal opercular formation in infants and children. AJNR Am J Neuroradiol 1996; 17 (07) 1303-1311
    PubMedGoogle Scholar
  • 18 Sanz-Cortes M, Egaña-Ugrinovic G, Zupan R, Figueras F, Gratacos E. Brainstem and cerebellar differences and their association with neurobehavior in term small-for-gestational-age fetuses assessed by fetal MRI. Am J Obstet Gynecol 2014; 210 (05) 452.e1-452.e8
    CrossrefPubMedGoogle Scholar
  • 19 Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 2012; 11 (02) 352-365
    CrossrefPubMedGoogle Scholar
  • 20 Achiron R, Kivilevitch Z, Lipitz S, Gamzu R, Almog B, Zalel Y. Development of the human fetal pons: in utero ultrasonographic study. Ultrasound Obstet Gynecol 2004; 24 (05) 506-510
    CrossrefPubMedGoogle Scholar
  • 21 Malinger G, Ginath S, Lerman-Sagie T, Watemberg N, Lev D, Glezerman M. The fetal cerebellar vermis: normal development as shown by transvaginal ultrasound. Prenat Diagn 2001; 21 (08) 687-692
    CrossrefPubMedGoogle Scholar
  • 22 Garel C. MRI of the Fetal Brain. Berlin, Germany: Springer-Verlag; 2004: 151-175
    CrossrefGoogle Scholar
  • 23 Triulzi F, Parazzini C, Righini A. MRI of fetal and neonatal cerebellar development. Semin Fetal Neonatal Med 2005; 10 (05) 411-420
    CrossrefPubMedGoogle Scholar
  • 24 Scott JA, Hamzelou KS, Rajagopalan V. , et al. 3D morphometric analysis of human fetal cerebellar development. Cerebellum 2012; 11 (03) 761-770
    CrossrefPubMedGoogle Scholar
  • 25 Yalin Imamoglu E, Gursoy T, Sancak S, Ovali F. Does being born small-for-gestational-age affect cerebellar size in neonates?. J Matern Fetal Neonatal Med 2016; 29 (06) 892-896
    CrossrefPubMedGoogle Scholar
  • 26 Nguyen The Tich S, Anderson PJ, Shimony JS, Hunt RW, Doyle LW, Inder TE. A novel quantitative simple brain metric using MR imaging for preterm infants. AJNR Am J Neuroradiol 2009; 30 (01) 125-131
    CrossrefPubMedGoogle Scholar
  • 27 Bertucci E, Gindes L, Mazza V, Re C, Lerner-Geva L, Achiron R. Vermian biometric parameters in the normal and abnormal fetal posterior fossa: three-dimensional sonographic study. J Ultrasound Med 2011; 30 (10) 1403-1410
    CrossrefPubMedGoogle Scholar
  • 28 Bingham PM, Zimmerman RA, McDonald-McGinn D, Driscoll D, Emanuel BS, Zackai E. Enlarged sylvian fissures in infants with interstitial deletion of chromosome 22q11. Am J Med Genet 1997; 74 (05) 538-543
    CrossrefPubMedGoogle Scholar
  • 29 Mitnick RJ, Bello JA, Shprintzen RJ. Brain anomalies in velo-cardio-facial syndrome. Am J Med Genet 1994; 54 (02) 100-106
    CrossrefPubMedGoogle Scholar
  • 30 Lynch DR, McDonald-McGinn DM, Zackai EH. , et al. Cerebellar atrophy in a patient with velocardiofacial syndrome. J Med Genet 1995; 32 (07) 561-563
    CrossrefPubMedGoogle Scholar
  • 31 Mahle WT, Tavani F, Zimmerman RA. , et al. An MRI study of neurological injury before and after congenital heart surgery. Circulation 2002; 106 (12, Suppl 1): I109-I114
    PubMedGoogle Scholar
  • 32 Glauser TA, Rorke LB, Weinberg PM, Clancy RR. Congenital brain anomalies associated with the hypoplastic left heart syndrome. Pediatrics 1990; 85 (06) 984-990
    PubMedGoogle Scholar
  • 33 Khalil A, Suff N, Thilaganathan B, Hurrell A, Cooper D, Carvalho JS. Brain abnormalities and neurodevelopmental delay in congenital heart disease: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2014; 43 (01) 14-24
    CrossrefPubMedGoogle Scholar
  • 34 Ortinau C, Alexopoulos D, Dierker D, Van Essen D, Beca J, Inder T. Cortical folding is altered before surgery in infants with congenital heart disease. J Pediatr 2013; 163 (05) 1507-1510
    CrossrefPubMedGoogle Scholar
  • 35 Clouchoux C, du Plessis AJ, Bouyssi-Kobar M. , et al. Delayed cortical development in fetuses with complex congenital heart disease. Cereb Cortex 2013; 23 (12) 2932-2943
    CrossrefPubMedGoogle Scholar
  • 36 Farzan F, Pascual-Leone A, Schmahmann JD, Halko M. Enhancing the temporal complexity of distributed brain networks with patterned cerebellar stimulation. Sci Rep 2016; 6 (06) 23599
    CrossrefPubMedGoogle Scholar
  • 37 De Smet HJ, Paquier P, Verhoeven J, Mariën P. The cerebellum: its role in language and related cognitive and affective functions. Brain Lang 2013; 127 (03) 334-342
    CrossrefPubMedGoogle Scholar
  • 38 Fabbro F, Moretti R, Bava A. Language impairments in patients with cerebellar lesions. J Neurolinguist 2000; 13 (02) 173-188
    CrossrefPubMedGoogle Scholar
  • 39 Gadgil N, Hansen D, Barry J, Chang R, Lam S. Posterior fossa syndrome in children following tumor resection: knowledge update. Surg Neurol Int 2016; 7 (06) (Suppl. 06) S179-S183
    CrossrefPubMedGoogle Scholar
  • 40 Puget S, Boddaert N, Viguier D. , et al. Injuries to inferior vermis and dentate nuclei predict poor neurological and neuropsychological outcome in children with malignant posterior fossa tumors. Cancer 2009; 115 (06) 1338-1347
    CrossrefPubMedGoogle Scholar
  • 41 Brossard-Racine M, du Plessis AJ, Vezina G. , et al. Prevalence and spectrum of in utero structural brain abnormalities in fetuses with complex congenital heart disease. AJNR Am J Neuroradiol 2014; 35 (08) 1593-1599
    CrossrefPubMedGoogle Scholar
  • 42 Borzage M, Blüml S, Seri I. Equations to describe brain size across the continuum of human lifespan. Brain Struct Funct 2014; 219 (01) 141-150
    CrossrefPubMedGoogle Scholar
  • 43 Rajagopalan V, Scott J, Habas PA. , et al. Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. J Neurosci 2011; 31 (08) 2878-2887
    CrossrefPubMedGoogle Scholar
  • 44 Li G, Nie J, Wang L. , et al. Mapping longitudinal hemispheric structural asymmetries of the human cerebral cortex from birth to 2 years of age. Cereb Cortex 2014; 24 (05) 1289-1300
    CrossrefPubMedGoogle Scholar
  • 45 Brouwer MJ, de Vries LS, Groenendaal F. , et al. New reference values for the neonatal cerebral ventricles. Radiology 2012; 262 (01) 224-233
    CrossrefPubMedGoogle Scholar
  • 46 Tilea B, Alberti C, Adamsbaum C. , et al. Cerebral biometry in fetal magnetic resonance imaging: new reference data. Ultrasound Obstet Gynecol 2009; 33 (02) 173-181
    CrossrefPubMedGoogle Scholar