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Learning and Memory in Adolescents With Critical Biventricular Congenital Heart Disease

Published online by Cambridge University Press:  20 June 2017

Adam R. Cassidy ,
Jane W. Newburger  and
David C. Bellinger
Adam R. Cassidy*
Affiliation:
Department of Psychiatry, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts
Jane W. Newburger
Affiliation:
Department of Cardiology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts
David C. Bellinger
Affiliation:
Departments of Neurology and Psychiatry, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts
*
Correspondence and reprint requests to: Adam R. Cassidy, Center for Neuropsychology, Department of Psychiatry, Boston Children’s Hospital, Boston, MA 02115. E-mail: adam.cassidy@childrens.harvard.edu
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Abstract

Objectives: Although evidence exists of broadly defined memory impairment among adolescents with critical congenital heart disease (CHD), nuanced investigations of declarative memory in this at-risk population have not been conducted. This study had two primary aims: (1) to conduct a fine-grained analysis of a range of relevant learning and memory processes in adolescents with critical biventricular CHD, and (2) to identify risk, odds, and predictors of memory impairment. Methods: Data were combined from two single-center studies of neurodevelopmental outcomes in critical CHD. Two-hundred seven adolescents (M age =15.61±1.0 years) with critical CHD (139 with dextro-transposition of the great arteries and 68 with tetralogy of Fallot without an identified genetic condition), as well as 61 healthy referents (M age =15.27±1.1 years) completed a neuropsychological evaluation which included the Children’s Memory Scale. Results: Whereas visual-spatial memory deficits were found in both CHD subgroups, verbal memory abilities were relatively preserved. Adolescents with CHD demonstrated stronger memory for Stories than Word Pairs, t (203)=2.63, p=.009, and for Dot Locations than Faces, t(204)=−2.57, p=.01. CHD subgroup, socioeconomic status, sex, and seizure history were among the most frequent significant predictors of memory impairment. Seizure history, in particular, was associated with a 2 to 3 times greater odds of impaired performance on learning and memory tasks. Conclusions: Adolescents with critical biventricular CHD are at risk for deficits in aspects of declarative memory. Independent risk factors for worse outcome include history of seizures. (JINS, 2017, 23, 627–639)

Keywords

MemoryRisk factorsCongenital heart defectCardiacAdolescentPediatric
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Issue 8 , September 2017 , pp. 627 - 639
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

REFERENCES

Bean Jaworski, J.L., White, M.T., DeMaso, D.R., Newburger, J.W., Bellinger, D.C., & Cassidy, A.R. (2017). Visuospatial processing in adolescents with critical congenital heart disease: Organization, integration, and implications for academic achievement. Child Neuropsychology, 0(0), 1–18. http://doi.org/10.1080/09297049.2017.1283396 Google Scholar
Beca, J., Gunn, J.K., Coleman, L., Hope, A., Reed, P.W., Hunt, R.W., & Shekerdemian, L.S. (2013). New white matter brain injury after infant heart surgery is associated with diagnostic group and the use of circulatory arrest. Circulation, 127(9), 971–979. http://doi.org/10.1161/CIRCULATIONAHA.112.001089 CrossRefGoogle ScholarPubMed
Begré, S., Frommer, A., von Känel, R., Kiefer, C., & Federspiel, A. (2007). Relation of white matter anisotropy to visual memory in 17 healthy subjects. Brain Research, 1168(1), 60–66. http://doi.org/10.1016/j.brainres.2007.06.096 Google Scholar
Bellinger, D.C., Bernstein, J.H., Kirkwood, M.W., Rappaport, L.A., & Newburger, J.W. (2003). Visual-spatial skills in children after open-heart surgery. Journal of Developmental and Behavioral Pediatrics, 24(3), 169–179.Google Scholar
Bellinger, D.C., Jonas, R.A., Rappaport, L.A., Wypij, D., Wernovsky, G., Kuban, K.C., & Strand, R.D. (1995). Developmental and neurologic status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. The New England Journal of Medicine, 332(9), 549–555. http://doi.org/10.1056/NEJM199503023320901 Google Scholar
Bellinger, D.C., & Newburger, J.W. (2010). Neuropsychological, psychosocial, and quality-of-life outcomes in children and adolescents with congenital heart disease. Progress in Pediatric Cardiology, 29(2), 87–92. http://doi.org/10.1016/j.ppedcard.2010.06.007 Google Scholar
Bellinger, D.C., Rappaport, L.A., Wypij, D., Wernovsky, G., & Newburger, J.W. (1997). Patterns of developmental dysfunction after surgery during infancy to correct transposition of the great arteries. Developmental and Behavioral Pediatrics, 18(2), 75–83.Google Scholar
Bellinger, D.C., Rivkin, M.J., DeMaso, D., Robertson, R.L., Stopp, C., Dunbar-Masterson, C., & Newburger, J.W. (2015). Adolescents with tetralogy of Fallot: Neuropsychological assessment and structural brain imaging. Cardiology in the Young, 25(2), 338–347. http://doi.org/10.1017/S1047951114000031 Google Scholar
Bellinger, D.C., Watson, C.G., Rivkin, M.J., Robertson, R.L., Roberts, A.E., Stopp, C., & Newburger, J.W. (2015). Neuropsychological Status and Structural Brain Imaging in Adolescents With Single Ventricle Who Underwent the Fontan Procedure. Journal of the American Heart Association, 4(12), e002302. http://doi.org/10.1161/JAHA.115.002302 Google Scholar
Bellinger, D.C., Wypij, D., DuPlessis, A.J., Rappaport, L.A., Jonas, R.A., Wernovsky, G., & Newburger, J.W. (2003). Neurodevelopmental status at eight years in children with dextro-transposition of the great arteries: The Boston Circulatory Arrest Trial. The Journal of Thoracic and Cardiovascular Surgery, 126(5), 1385–1396. http://doi.org/10.1016/S0022-5223(03)00711-6 Google Scholar
Bellinger, D.C., Wypij, D., Kuban, K.C.K., Rappaport, L.A., Hickey, P.R., Wernovsky, G., & Newburger, J.W. (1999). Developmental and neurological status of children at 4 years of age after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. Circulation, 100(5), 526–532. http://doi.org/10.1161/01.CIR.100.5.526 Google Scholar
Bellinger, D.C., Wypij, D., Rivkin, M.J., DeMaso, D.R., Robertson, R.L., Dunbar-Masterson, C., & Newburger, J.W. (2011). Adolescents with d-transposition of the great arteries corrected with the arterial switch procedure: Neuropsychological assessment and structural brain imaging. Circulation, 124(12), 1361–1369. http://doi.org/10.1161/CIRCULATIONAHA.111.026963 CrossRefGoogle ScholarPubMed
Brewster, R.C., King, T.Z., Burns, T.G., Drossner, D.M., & Mahle, W.T. (2015). White matter integrity dissociates verbal memory and auditory attention span in emerging adults with congenital heart disease. Journal of the International Neuropsychological Society, 21, 22–33. http://doi.org/10.1017/S135561771400109X CrossRefGoogle ScholarPubMed
Cassidy, A.R., White, M.T., DeMaso, D.R., Newburger, J.W., & Bellinger, D.C. (2015). Executive function in children and adolescents with critical cyanotic congenital heart disease. Journal of the International Neuropsychological Society, 20, 34–49. http://doi.org/10.1017/S1355617714001027 Google Scholar
Cassidy, A.R., White, M.T., DeMaso, D.R., Newburger, J.W., & Bellinger, D.C. (2016). Processing speed, executive function, and academic achievement in children with dextro-transposition of the great arteries: Testing a longitudinal developmental cascade model. Neuropsychology, 30, 874–885.CrossRefGoogle ScholarPubMed
Cohen, M. (1997). Children’s Memory Scale. San Antonio, TX: The Psychological Corporation.Google Scholar
Davachi, L., Mitchell, J., & Wagner, A. (2003). Multiple routes to memory: Distinct medial temporal lobe processes build itemandsource memories. Proceedings of the National Academy of Sciences of the United States of America, 100, 2157–2162.Google Scholar
DeMaso, D.R., Calderon, J., Taylor, G.A., Holland, J.E., Stopp, C., White, M.T., & Newburger, J.W. (2017). Psychiatric disorders in adolescents with single ventricle congenital heart disease. Pediatrics, 139(3), e20162241. http://doi.org/10.1542/peds.2016-2241.Google Scholar
DeMaso, D.R., Labella, M., Taylor, G.A., Forbes, P.W., Stopp, C., Bellinger, D.C., & Newburger, J.W. (2014). Psychiatric disorders and function in adolescents with d-transposition of the great arteries. Journal of Pediatrics, 165(4), 760–766. http://doi.org/10.1016/j.jpeds.2014.06.029 CrossRefGoogle ScholarPubMed
Dennis, M., Francis, D.J., Cirino, P.T., Schachar, R., Barnes, M.A., & Fletcher, J.M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society, 15(3), 331–343. http://doi.org/10.1017/S1355617709090481 Google Scholar
Eichenbaum, H. (2016). Memory: Organization and control. Annual Review of Psychology, 68, 19–45. http://doi.org/10.1146/annurev-psych-010416-044131 Google Scholar
Eichenbaum, H., Yonelinas, A., & Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123–152.Google Scholar
Evans, A.C. (2006). The NIH MRI study of normal brain development. Neuroimage, 30(1), 184–202. http://doi.org/10.1016/j.neuroimage.2005.09.068 Google Scholar
Gaynor, J.W., Stopp, C., Wypij, D., Andropoulos, D.B., Atallah, J., Atz, A.M., & Newburger, J.W. (2016). Impact of operative and postoperative factors on neurodevelopmental outcomes after cardiac operations. Annals of Thoracic Surgery, 102(3), 843–849. http://doi.org/10.1016/j.athoracsur.2016.05.081 Google Scholar
Gunn, J.K., Beca, J., Hunt, R.W., Olischar, M., & Shekerdemian, L.S. (2012). Perioperative amplitude-integrated EEG and neurodevelopment in infants with congenital heart disease. Intensive Care Medicine, 38(9), 1539–1547. http://doi.org/10.1007/s00134-012-2608-y Google Scholar
Hoffman, J.I.E., & Kaplan, S. (2002). The incidence of congenital heart disease. Journal of the American College of Cardiology, 39(12), 1890–1900.Google Scholar
Holland, J.E., Cassidy, A.R., Stopp, C., White, M.T., Bellinger, D.C., Rivkin, M.J., & DeMaso, D.R. (in press). Psychiatric disorders and function in adolescents with tetralogy of Fallot. The Journal of Pediatrics.Google Scholar
Karsdorp, P.A., Everaerd, W., Kindt, M., & Mulder, B.J.M. (2007). Psychological and cognitive functioning in children and adolescents with congenital heart disease: A meta-analysis. Journal of Pediatric Psychology, 32(5), 527–541. http://doi.org/10.1093/jpepsy/jsl047 Google Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., & Ryan, N. (1997). Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 980–988.CrossRefGoogle ScholarPubMed
Marelli, A., Miller, S.P., Marino, B.S., Jefferson, A.L., & Newburger, J.W. (2016). Brain in congenital heart disease across the lifespan. Circulation, 133(20), 1951–1962. http://doi.org/10.1161/CIRCULATIONAHA.115.019881 Google Scholar
Marino, B.S., Lipkin, P.H., Newburger, J.W., Peacock, G., Gerdes, M., Gaynor, J.W., & Mahle, W.T. (2012). Neurodevelopmental outcomes in children with congenital heart disease: Evaluation and management: A scientific statement from the American Heart Association. Circulation, 126(9), 1143–1172. http://doi.org/10.1161/CIR.0b013e318265ee8a Google Scholar
Miatton, M., De Wolf, D., François, K., Thiery, E., & Vingerhoets, G. (2007a). Intellectual, neuropsychological, and behavioral functioning in children with tetralogy of Fallot. The Journal of Thoracic and Cardiovascular Surgery, 133(2), 449–455. http://doi.org/10.1016/j.jtcvs.2006.10.006 Google Scholar
Miatton, M., De Wolf, D., François, K., Thiery, E., & Vingerhoets, G. (2007b). Neuropsychological performance in school-aged children with surgically corrected congenital heart disease. The Journal of Pediatrics, 151(1), 73–78, 78.e1. http://doi.org/10.1016/j.jpeds.2007.02.020 Google Scholar
Newburger, J.W., Jonas, R.A., Wernovsky, G., Wypij, D., Hickey, P.R., Kuban, K.C.K.,&Ware, J.H. (1993). A comparison of the perioperative neurologic effects of hypothermic circulatory arrest versus low-flow cardiopulmonary bypass in infant heart surgery. New England Journal of Medicine, 329(15), 1057–1064.Google Scholar
Pierpont, E.I., Tworog-Dube, E., & Roberts, A.E. (2013). Learning and memory in children with Noonan syndrome. American Journal of Medical Genetics. Part A, 161(9), 2250–2257. http://doi.org/10.1002/ajmg.a.36075 Google Scholar
Puka, K., & Smith, M.L. (2016). Remembrance and time passed: Memory outcomes 4-11 years after pediatric epilepsy surgery. Epilepsia, 1–10. http://doi.org/10.1111/epi.13571 Google ScholarPubMed
Rappaport, L.A., Wypij, D., Bellinger, D.C., Helmers, S.L., Holmes, G.L., Barnes, P.D., & Newburger, J.W. (1998). Relation of seizures after cardiac surgery in early infancy to neurodevelopmental outcome. Circulation, 97(8), 773–779. http://doi.org/10.1161/01.CIR.97.8.773 Google Scholar
Reller, M.D., Strickland, M.J., Riehle-Colarusso, T., Mahle, W.T., & Correa, A. (2008). Prevalence of congenital heart defects in metropolitan Atlanta, 1998-2005. Journal of Pediatrics, 153(6), 807–813. http://doi.org/10.1016/j.jpeds.2008.05.059 CrossRefGoogle ScholarPubMed
Rollins, C.K., Asaro, L.A., Akhondi-Asl, A., Kussman, B.D., Rivkin, M.J., Bellinger, D.C., & Soul, J.S. (2016). White matter volume predicts language development in congenital heart disease. The Journal of Pediatrics, 181, 42–48.e2. http://doi.org/10.1016/j.jpeds.2016.09.070 Google Scholar
Rollins, C.K., Watson, C.G., Asaro, L.A., Wypij, D., Vajapeyam, S., Bellinger, D.C., & Rivkin, M.J. (2014). White matter microstructure and cognition in adolescents with congenital heart disease. The Journal of Pediatrics, 165(5), 936–944.e2. http://doi.org/10.1016/j.jpeds.2014.07.028 Google Scholar
Sanz, J.H., Berl, M.M., Armour, A.C., Wang, J., Cheng, Y.I., & Donofrio, M.T. (2016). Prevalence and pattern of executive dysfunction in school age children with congenital heart disease. Congenital Heart Disease, 12, 202–209. http://doi.org/10.1111/chd.12427 Google Scholar
Schaefer, C., von Rhein, M., Knirsch, W., Huber, R., Natalucci, G., Caflisch, J., & Latal, B. (2013). Neurodevelopmental outcome, psychological adjustment, and quality of life in adolescents with congenital heart disease. Developmental Medicine and Child Neurology, 55(12), 1143–1149. http://doi.org/10.1111/dmcn.12242 Google Scholar
Sun, L., Macgowan, C.K., Sled, J.G., Yoo, S.J., Manlhiot, C., Porayette, P., & Seed, M. (2015). Reduced fetal cerebral oxygen consumption is associated with smaller brain size in fetuses with congenital heart disease. Circulation, 131(15), 1313–1323. http://doi.org/10.1161/CIRCULATIONAHA.114.013051 CrossRefGoogle ScholarPubMed
Unger, A., Alm, K.H., Collins, J.A., O’Leary, J.M., & Olson, I.R. (2016). Variation in white matter connectivity predicts the ability to remember faces and discriminate their emotions. Journal of the International Neuropsychological Society, 22(2), 180–190. http://doi.org/10.1017/S1355617715001009 CrossRefGoogle ScholarPubMed
Volpe, J.J. (2014). Encephalopathy of congenital heart disease- Destructive and developmental effects intertwined. Journal of Pediatrics, 164(5), 962–965. http://doi.org/10.1016/j.jpeds.2014.01.002 Google Scholar
Volpe, J.J., Kinney, H.C., Jensen, F.E., & Rosenberg, P.A. (2011). The developing oligodendrocyte: Key cellular target in brain injury in the premature infant. International Journal of Developmental Neuroscience, 29(6), 565–582. http://doi.org/10.1016/j.ijdevneu.2011.07.008 Google Scholar
Waber, D.P., De Moor, C., Forbes, P.W., Almli, C.R., Botteron, K.N., Leonard, G., & Rumsey, J. (2007). The NIH MRI study of normal brain development: Performance of a population based sample of healthy children aged 6 to 18 years on a neuropsychological battery. Journal of the International Neuropsychological Society, 13(5), 729–746. http://doi.org/10.1017/S1355617707070841 Google Scholar