Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T08:18:30.210Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurobehavioral impact of sickle cell disease in early childhood

Published online by Cambridge University Press:  18 October 2007

JEFFREY SCHATZ  and
CARLA W. ROBERTS
JEFFREY SCHATZ
Affiliation:
Department of Psychology, University of South Carolina, Columbia, South Carolina Department of Pediatrics, University of South Carolina, Columbia, South Carolina
CARLA W. ROBERTS
Affiliation:
Department of Pediatrics, University of South Carolina, Columbia, South Carolina
Get access Rights & Permissions [Opens in a new window]

Abstract

The physical effects of sickle cell disease (SCD) begin in infancy or early childhood, yet most behavioral studies have focused on school-age children. We evaluated the impact of higher versus lower neurologic risk on language, motor abilities, executive functions, and temperament in toddlers and early preschoolers with SCD. Thirty-nine children with higher risk SCD were compared to 22 children with lower risk SCD. Language and motor abilities were lower in older compared with younger children but were unrelated to sickle cell subgroups. Executive functions, particularly working memory, were poorer in children with higher risk SCD regardless of age. Parent-reported activity level was also lower in children with higher risk. Specific behavioral influences of SCD are evident early in childhood and include working memory decrements. Executive function deficits in SCD can emerge early in life and may be an important context for other areas of cognitive and behavioral development. (JINS, 2007, 13, 933–943.)

Keywords

Child developmentChronic diseaseLanguage developmentMemoryShort-termNeurologic manifestationsTemperament
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 13 , Issue 6 , November 2007 , pp. 933 - 943
Copyright
© 2007 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amer, J., Ghoti, H., Rachmilewitz, E., Koren, A., Levin, C., & Fibach, E. (2006). Red blood cells, platelets and polymorphonuclear neutrophils of patients with sickle cell disease exhibit oxidative stress that can be ameliorated by antioxidants. British Journal of Haematology, 132, 108–113.Google Scholar
Armstrong, F.D., Thompson, R.J., Wang, W.C., Zimmerman, R., Pegelow, C.H., Miller, S., Moser, F., Bello, J., Hurtig, A., & Vass, K. (1996). Cognitive functioning and brain magnetic resonance imaging in children with sickle cell disease. Pediatrics, 97, 864–870.Google Scholar
Aylward, G.P. (1995). The Bayley Infant Neurodevelopmental Screener. San Antonio, TX: The Psychological Corporation.
Barden, E.M., Zemel, B.S., Kawchak, D.A., Goran, M.I., Ohene-Frempong, K., & Stallings, V.A. (2000). Total and resting energy expenditure in children with sickle cell disease. Journal of Pediatrics, 136, 73–79.Google Scholar
Bayley, N. (1993). Bayley Scales of Infant Development, Second Edition. San Antonio, TX: The Psychological Corporation.
Bernaudin, F., Verlhac, S., Freard, F., Roudot-Thoraval, F., Benkerrou, M., Thuret, I., Mardini, R., Vannier, J.P., Ploix, E., Romero, M., Casse-Perrot, C., Helly, M., Gillard, E., Sebag, G., Kchouk, H., Pracros, J.P., Finck, B., Dacher, J.N., Ickowicz, V., Raybaud, C., Poncet, M., Lesprit, E., Renert, P.H., & Brugieres, P. (2000). Multicenter prospective study of children with sickle cell disease: Radiographic and psychometric correlation. Journal of Child Neurology, 15, 333–343.Google Scholar
Blair, C., Peters, R., & Granger, D. (2004). Physiological and neuropsychological correlates of approach/withdrawal tendencies in preschool: further examination of the behavioral inhibition system/behavioral activation system scales for young children. Developmental Psychobiology, 45, 113–124.Google Scholar
Bradley, R.H., Corwyn, R.F., & Burchinal, M. (2001). The home environments of children in the United States Part II: Relations with behavioral development through age thirteen. Child Development, 72, 1868–1886.Google Scholar
Brandling-Bennett, E.M., White, D.A., Armstrong, M.M., Christ, S.E., & DeBaun, M.R. (2003). Patterns of verbal long-term and working memory performance reveal deficits in strategic processing in children with frontal infarcts related to sickle cell disease. Developmental Neuropsychology, 24, 423–434.Google Scholar
Brooks, L.J., Koziol, S.M., Chiarucci, K.M., & Berman, B.W. (1996). Does sleep-disordered breathing contribute to the clinical severity of sickle cell anemia? Journal of Pediatric Hematology/Oncology, 18, 135–139.Google Scholar
Brown, R.T., Buchanan, I., Doepke, K., Eckman, J.R., Baldwin, K., Goonan, B., & Schoenher, S. (1993). Cognitive and academic functioning in children with sickle cell disease. Journal of Clinical Child Psychology, 22, 207–218.Google Scholar
Buss, A. & Plomin, R. (1984). Temperament: Early personality traits. Hillsdale, N.J.: Erlbaum.
Caldwell, B.M. & Bradley, R.H. (1979). Home observation for measurement of the environment. Little Rock: University of Arkansas at Little Rock.
Calkins, S.D. (1997). Cardiac vagal tone indices of temperamental reactivity and behavioral regulation in young children. Developmental Psychobiology, 31, 125–135.Google Scholar
Clarke, L.A. & Watson, D. (1995). Constructing validity: Basic issues in objective scale development. Psychological Assessment, 7, 309–319.Google Scholar
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences. Hillsdale, NJ: Lawrence Erlbaum Associates.
Cohen, S. (1986). Contrasting the hassles scale and the perceived stress scale: Who's really measuring appraised stress? American Psychologist, 41, 717–718.Google Scholar
Cohen, S., Kamarck, T., & Mermelstein, R. (1983). A global measure of perceived stress. Journal of Health and Social Behavior, 24, 385–396.Google Scholar
Cohen, S. & Williamson, G.M. (1987). Perceived stress in a probability sample of the United States. In S. Spacapan & S. Oskamp (Eds.), The Social Psychology of Health (pp. 31–67). Newbury Park: Sage Publications.
Coons, C.E., Gay, E.C., Fandal, A.W., Ker, C., & Frankenburg, W.K. (1981). The Home Screening Questionnaire reference manual. Denver: Denver Developmental Materials.
Dale, P.S., Reznick, J.S., Thal, D., & Marchman, V.A. (2001). A parent report measure of language development for three-year-olds. Unpublished manuscript, University of Missouri–Columbia.
Derryberry, D. & Rothbart, M.K. (1997). Reactive and effortful processes in the organization of temperament. Development and Psychopathology, 9, 633–652.Google Scholar
Diamond, A. (1988). The abilities and neural mechanisms underlying AB performance. Child Development, 59, 523–527.Google Scholar
Diamond, A. & Goldman-Rakic, P.S. (1989). Comparison of human infants and rhesus monkeys on Piaget's AB task: Evidence for dependence on dorsolateral prefrontal cortex. Experimental Brain Research, 74, 24–40.Google Scholar
Dumka, L.E., Stoerzinger, H.D., Jackson, K.M., & Roosa, M.W. (1996). Examination of the cross-cultural and cross-language equivalence of the Parenting Self-Agency Measure. Family Relations, 45, 216–222.Google Scholar
Espy, K.A., Kaufmann, P.M., & Glisky, M.L. (1999b). Neuropsychologic function in toddlers exposed to cocaine in utero: A preliminary study. Developmental Neuropsychology, 15, 447–460.Google Scholar
Espy, K.A., Kaufmann, P.M., McDiarmid, M.D., & Glisky, M.L. (1999a). Executive functioning in preschool children: Performance on A-not-B and other delayed response format tasks. Brain and Cognition, 41, 178–199.Google Scholar
Faraci, F.M. (2005). Oxidative stress: the curse that underlies cerebral vascular dysfunction? Stroke, 36, 186–188.Google Scholar
Fenson, L., Pethick, S., & Renda, C. (2000). Short-form versions of the MacArthur Communicative Development Inventories. Applied Psycholinguistics, 21, 95–115.Google Scholar
Frankenburger, W.K., Dodds, J., Archer, P., Bresnick, B., Maschka, P., Edelman, AN., & Shapiro, H. (1996). Denver II Technical Manual. Denver, CO: Denver Developmental Materials, Inc.
Gartstein, M.A. & Rothbart, M.K. (2003). Studying infant temperament via the Revised Infant Behavior Questionnaire. Infant Behavior and Development, 166, 1–23.Google Scholar
Glascoe, F.P., Byrne, K.E., & Ashford, L.G. (1992). Accuracy of the Denver-II in developmental screening. Pediatrics, 89, 1221–1225.Google Scholar
Gray, N.T., Bartlett, J.M., Kolasa, K.M., Marcuard, S.P., Holbrook, C.T., & Horner, R.D. (1992). Nutritional status and dietary intake of children with sickle cell anemia. American Journal of Pediatric Hematology/Oncology, 14, 57–61.Google Scholar
Greer, S., Bauchner, H., & Zuckerman, B. (1989). The Denver Developmental Screening Test: How good is its predictive validity? Developmental Medicine and Child Neurology, 31, 774–781.Google Scholar
Gunnar, M.R., Porter, F.L., Wolf, C.M., Rigatuso, J., & Larson, M.C. (1995). Neonatal stress reactivity: Predictions to later emotional temperament. Child Development, 66, 1–13.Google Scholar
Hill, C.M., Hogan, A.M., Onugha, N., Harrison, D., Cooper, S., McGrigor, V.J., Datta, A., & Kirkham, F.J. (2006). Increased cerebral blood flow velocity in children with mild sleep-disordered breathing: A possible association with abnormal neuropsychological function. Pediatrics, 118, 1100–1108.Google Scholar
Hogan, A.M., Kirkham, F.J., Prengler, M., Telfer, P., Lane, R., Vargha-Khadem, F., & Haan, M. (2006). An exploratory study of physiological correlates of neurodevelopmental delay in infants with sickle cell anaemia. British Journal of Haematology, 132, 99–107.Google Scholar
Key, J.D., Brown, R.T., & Marsh, L.D. (2001). Depressive symptoms in adolescents with a chronic illness. Children's Health Care, 30, 283–292.Google Scholar
Kirkham, F.J., Calamante, F., Bynevelt, M., Gadian, D.G., Evans, J.P., Cox, T.C., & Connelly A. (2001b). Perfusion magnetic resonance abnormalities in patients with sickle cell disease. Annals of Neurology, 49, 477–485.Google Scholar
Kirkham, F.J., Hewes, D.K., Prengler, M., Wade, A., Lane, R., & Evans, J.P. (2001a). Nocturnal hypoxaemia and central-nervous-system events in sickle-cell disease. Lancet, 357, 1656–1659.Google Scholar
Locke, A. & Ginsborg, J. (2003). Spoken language in the early years: The cognitive and linguistic development of three- to five-year-old children from socio-economically deprived backgrounds. Educational and Child Psychology, 20, 68–79.Google Scholar
Mathiesen, K.S. & Tambs, K. (1999). The EAS Temperament Questionnaire–factor structure, age trends, reliability, and stability in a Norwegian sample. Journal of Child Psychology and Psychiatry, 40, 431–439.Google Scholar
McMahon, R., Lengua, L., & Kim, H. (1996). Parent Questionnaire (Fast Track Technical Report). Seattle, WA: University of Washington.
Meisels, S.J. (1989). Can developmental screening tests identify children who are developmentally at risk? Pediatrics, 83, 578–585.Google Scholar
Moser, F.G., Miller, S.T., Bello, J.A., Pegelow, C.H., Zimmerman, R.A., Wang, W.C., Ohene-Frempong, K., Schwartz, A., Vichinsky, E.P., Gallagher, D., & Kinney, T.R. (1996). The spectrum of brain MR abnormalities in sickle-cell disease: A report from the Cooperative Study of Sickle Cell Disease. American Journal of Neuroradiology, 17, 965–972.Google Scholar
Nahavandi, M., Tavakkoli, F., Hasan, S.P., Wyche, M.Q., & Castro, O. (2004). Cerebral oximetry in patients with sickle cell disease. European Journal of Clinical Investigation, 34, 143–148.Google Scholar
Noll, R.B., Stith, L., Gartstein, M.A., Ris, M.D., Grueneich, R., Vannatta, K., & Kalinyak, K. (2001). Neuropsychological functioning of youths with sickle cell disease: comparison with non-chronically ill peers. Journal of Pediatric Psychology, 26, 69–78.Google Scholar
Oguz, K.K., Golay, X., Pizzini, F.B., Freer, C.A., Winrow, N., Ichord, R., Casella, J.F., van Zijl, P.C., & Melhem, E.R. (2003). Sickle cell disease: Continuous arterial spin-labeling perfusion MR imaging in children. Radiology, 227, 567–574.Google Scholar
Ohene-Frempong, K., Weiner, S.J., Sleeper, L.A., Miller, S.T., Embury, S., Moohr, J.W., Wethers, D.L., Pegelow, C.H., & Gill, F.M. (1998). Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood, 91, 288–294.Google Scholar
Pearson, S.R., Alkon, A., Treadwell, M., Wolff, B., Quirolo, K., & Boyce, W.T. (2005). Autonomic reactivity and clinical severity in children with sickle cell disease. Clinical Autonomic Research, 15, 400–407.Google Scholar
Pegelow, C.H., Macklin, E.A., Moser, F.G., Wang, W.C., Bello, J.A., Miller, S.T., Vichinsky, E.P., DeBaun, M.R., Guarini, L., Zimmerman, R.A., Younkin, D.P., Gallagher, D.M., & Kinney, T.R. (2002). Longitudinal changes in brain magnetic resonance imaging findings in children with sickle cell disease. Blood, 99, 3014–3018.Google Scholar
Posner, M.I. & Rothbart, M.K. (1998). Summary and commentary: Developing attentional skills. In J.E. Richards (Ed.), Cognitive neuroscience of attention: A developmental perspective (pp. 317–323). Mahwah, NJ: Erlbaum.
Robertson, P.L., Aldrich, M.S., Hanash, S.M., & Goldstein, G.W. (1988). Stroke associated with obstructive sleep apnea in a child with sickle cell anemia. Annals of Neurology, 23, 614–616.Google Scholar
Rothbart, M.K., Ahadi, S.A., & Hersey, K.L. (2001). Investigations of temperament at three to seven years: The Children's Behavior Questionnaire. Child Development, 72, 1394–1408.CrossRefGoogle Scholar
Rothbart, M.K., Ellis, L.K., & Rueda, M.R. (2003). Developing mechanisms of temperamental effortful control. Journal of Personality, 71, 1113–1143.Google Scholar
Rowe, D.C. & Plomin, R. (1977). Temperament in early childhood. Journal of Personality Assessment, 41, 150–156.Google Scholar
Sanson, A. & Rothbart, M.K. (1995). Child temperament and parenting. In M. Bornstein (Ed.), Handbook of Parenting, Vol. 4 (pp. 299–321). Hillsdale, NJ: Lawrence Earlbaum.
Schatz, J. (2004a). Brief report: Academic attainment in children with sickle cell disease. Journal of Pediatric Psychology, 29, 627–633.Google Scholar
Schatz, J., Brown, R.T., Pascual, J.M., Hsu, L., & DeBaun, M.R. (2001). Poor school and cognitive functioning with silent cerebral infarction and sickle cell disease. Neurology, 56, 1109–1111.Google Scholar
Schatz, J., Finke, R.L., Kellett, J.M., & Kramer, J.H. (2002). Cognitive functioning in children with sickle cell disease: A meta-analysis. Journal of Pediatric Psychology, 8, 739–748.Google Scholar
Schatz, J., Finke, R.L., & Roberts, C.W. (2004b). Interactions among biomedical and environmental factors in cognitive development: A preliminary study of sickle cell disease. Journal of Developmental and Behavioral Pediatrics, 25, 303–310.Google Scholar
Schatz, J., McClellan, C.B., Puffer, E., Johnson, K., & Roberts, C.W., (in press). Neurodevelopmental screening in toddlers and early preschoolers with sickle cell disease. Journal of Child Neurology.
Sindel, L.J., Dishuck, J.F., Baliga, B.S., & Mankad, V.N. (1990). Micronutrient deficiency and neutrophil function in sickle cell disease. Annals of the New York Academy of Sciences, 587, 70–77.Google Scholar
Singhal, A., Davies, P., Wierenga, K.J., Thomas, P., & Serjeant, G. (1997). Is there an energy deficiency in homozygous sickle cell disease? American Journal of Clinical Nutrition, 66, 386–390.Google Scholar
Singhal, A., Parker, S., Linsell, L., & Serjeant, G. (2002). Energy intake and resting metabolic rate in preschool Jamaican children with homozygous sickle cell disease. American Journal of Clinical Nutrition, 75, 1093–1097.Google Scholar
Sparrow, S., Balla, D.A., & Cicchetti, D.V. (1984). Vineland Adaptive Behavior Scales, Survey Edition. Circle Pines, MN: American Guidance Service.
Steen, R.G., Fineberg-Buchner, C., Hankins, G., Weiss, L., Prifitera, A., & Mulhern, R.K. (2005). Cognitive deficits in children with sickle cell disease. Journal of Child Neurology, 20, 102–107.Google Scholar
Steinberg, M.H. (1984). Review: the sickle hemoglobinopathies–genetic analyses of common phenocopies and new molecular approaches to treatment. American Journal of the Medical Sciences, 288, 169–174.Google Scholar
Strayhorn, J.M. & Weidman, C.S. (1988). A parenting practices scale and its relation to parent and child mental health. Journal of the American Academy of Child and Adolescent Psychiatry, 27, 613–618.Google Scholar
Thompson, R.J., Jr., Armstrong, F.D., Link, C.L., Pegelow, C.H., Moser, F., & Wang, W.C. (2003). A prospective study of the relationship over time of behavior problems, intellectual functioning, and family functioning in children with sickle cell disease: A report from the cooperative study of sickle cell disease. Journal of Pediatric Psychology, 28, 59–65.Google Scholar
Thompson, R.J., Jr., Gustafson, K.E., Bonner, M.J., & Ware, R.E. (2002). Neurocognitive development of young children with sickle cell disease through three years of age. Journal of Pediatric Psychology, 27, 235–244.Google Scholar
Wali, Y.A., Al-Lamki, Z., Soliman, H., & Al-Okbi, H. (2000). Adenotonsillar Hypertrophy: A precipitating factor of cerebrovascular accident in a child with sickle cell anemia. Journal of Tropical Pediatrics, 46, 246–248.Google Scholar
Wang, W., Enos, L., Gallagher, D., Thompson, R., Guarini, L., Vichinsky, E., Wright, E., Zimmerman, R., & Armstrong, F.D. (2001). Neuropsychologic performance in school-aged children with sickle cell disease: A report from the Cooperative Study of Sickle Cell Disease. Journal of Pediatrics, 139, 391–397.Google Scholar
Wang, W.C., Grover, R., Gallagher, D., Espeland, M., & Fandal, A. (1993). Developmental screening in young children with sickle cell disease. The American Journal of Pediatric Hematology/Oncology, 15, 87–91.CrossRefGoogle Scholar
Wang, W.C., Langston, J.W., Steen, R.G., Wynn, L.W., Mulhern, R.K., Wilimas, J.A., Kim, F.M., & Figueroa, R.E. (1998). Abnormalities of the central nervous system in very young children with sickle cell anemia. Journal of Pediatrics, 132, 994–998.Google Scholar
Wood, K.C., Hebbel, R.P., & Granger, D.N. (2005). Endothelial cell NADPH oxidase mediates the cerebral microvascular dysfunction in sickle cell transgenic mice. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 19, 989–991.Google Scholar