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Neurodevelopmental Outcomes in Preterm Children with Sickle Cell Disease

Published online by Cambridge University Press:  29 November 2021

Sarah E. Bills Open the ORCID record for Sarah E. Bills [Opens in a new window] ,
Jeffrey Schatz Open the ORCID record for Jeffrey Schatz [Opens in a new window] ,
Erin Hunt ,
Sreya Varanasi ,
Julia Johnston  and
Jessica Bradshaw
Sarah E. Bills*
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
Jeffrey Schatz
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
Erin Hunt
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
Sreya Varanasi
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
Julia Johnston
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
Jessica Bradshaw
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
*
*Correspondence and reprint requests to: Sarah E. Bills, M.A., Department of Psychology, University of South Carolina, Columbia, SC, 29208, USA. E-mail: sbills@email.sc.edu
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Abstract

Objectives:

To explore the combined effect of pediatric sickle cell disease (SCD) and preterm birth on cognitive functioning.

Methods:

Cognitive functioning was examined in children ages 6–8 with high risk SCD genotypes born preterm (n = 20) and full-term (n = 59) and lower risk SCD genotypes/no SCD born preterm (n = 11) and full-term (n = 99) using tests previously shown to be sensitive to SCD-related neurocognitive deficits. Factorial ANOVAs and log linear analyses were conducted to examine the relationship between SCD risk, preterm birth status, and cognitive outcomes. Continuous scores were examined for specific tests. Children were categorized as having an abnormal screening outcome if at least one cognitive score was ≥1.5 standard deviations below the population mean.

Results:

Children with elevated risk due to high risk SCD and preterm birth performed worse than other groups on a test of expressive language but not on tests that emphasize processing speed and working memory. There was a three-way interaction between preterm status, SCD risk, and abnormal screening outcome, which was largely driven by the increased likelihood of abnormal cognitive scores for children with high risk SCD born preterm.

Conclusions:

The combination of SCD and preterm birth may confer increased risk for language deficits and elevated rates of abnormal cognitive screenings. This suggests that neurodevelopmental risk imparted by comorbid SCD and preterm birth may manifest as heterogenous, rather than specific, patterns of cognitive deficits. Future studies are needed to clarify the domains of cognitive functioning most susceptible to disease-related effects of comorbid SCD and preterm birth.

Keywords

Premature birthcognitive functioningdouble hitchronic illnessbrain developmentneurocognitive risk
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 10 , November 2022 , pp. 1039 - 1049
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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References

REFERENCES

Aarnoudse-Moens, C.S.H., Weisglas-Kuperus, N., van Goudoever, J.B., & Oosterlaan, J. (2009). Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics, 124(2), 717–728.CrossRefGoogle ScholarPubMed
Allotey, J., Zamora, J., Cheong-See, F., Kalidindi, M., Arroyo-Manzano, D., Asztalos, E. … Birtles, D. (2018). Cognitive, motor, behavioural and academic performances of children born preterm: A meta-analysis and systematic review involving 64 061 children. BJOG: An International Journal of Obstetrics & Gynaecology, 125(1), 16–25.CrossRefGoogle ScholarPubMed
Anderson, V., Spencer-Smith, M., & Wood, A. (2011). Do children really recover better? Neurobehavioural plasticity after early brain insult. Brain, 134(8), 2197–2221.CrossRefGoogle ScholarPubMed
Aylward, G.P. (2002). Cognitive and neuropsychological outcomes: More than IQ scores. Mental Retardation and Developmental Disabilities Research Reviews, 8(4), 234–240.CrossRefGoogle ScholarPubMed
Bakri, M.H., Ismail, E.A., Elsedfy, G.O., Amr, M.A., & Ibrahim, A. (2014). Behavioral impact of sickle cell disease in young children with repeated hospitalization. Saudi Journal of Anaesthesia, 8(4), 504.CrossRefGoogle ScholarPubMed
Barbarin, O.A. & Christian, M. (1999). The social and cultural context of coping with sickle cell disease: I. A review of biomedical and psychosocial issues. Journal of Black Psychology, 25(3), 277–293.CrossRefGoogle Scholar
Baron, I.S. & Rey-Casserly, C. (2010). Extremely preterm birth outcome: A review of four decades of cognitive research. Neuropsychology Review, 20(4), 430–452.CrossRefGoogle ScholarPubMed
Batalle, D., Hughes, E.J., Zhang, H., Tournier, J.-D., Tusor, N., Aljabar, P. …, Nosarti, C. (2017). Early development of structural networks and the impact of prematurity on brain connectivity. Neuroimage, 149, 379–392.CrossRefGoogle ScholarPubMed
Beery, K.E. (2004). The Beery-Buktenica Developmental Test of Visual-Motor Integration: Beery VMI, with Supplemental Developmental Tests of Visual Perception and Motor Coordination, and Stepping Stones Age Norms from Birth to Age Six. Minneapolis, MN: NCS Pearson.Google Scholar
Belanger, H.G., Spiegel, E., & Vanderploeg, R.D. (2010). Neuropsychological performance following a history of multiple self-reported concussions: A meta-analysis. Journal of the International Neuropsychological Society: JINS, 16(2), 262.CrossRefGoogle ScholarPubMed
Berkelhammer, L.D., Williamson, A.L., Sanford, S.D., Dirksen, C.L., Sharp, W.G., Margulies, A.S., & Prengler, R.A. (2007). Neurocognitive sequelae of pediatric sickle cell disease: A review of the literature. Child Neuropsychology, 13(2), 120–131.CrossRefGoogle ScholarPubMed
Bernaudin, F., Verlhac, S., Arnaud, C., Kamdem, A., Chevret, S., Hau, I., & Lesprit, E. (2011). Impact of early transcranial Doppler screening and intensive therapy on cerebral vasculopathy outcome in a newborn sickle cell anemia cohort. Blood, 117(4), 1130–1140.CrossRefGoogle Scholar
Bernaudin, F., Verlhac, S., Arnaud, C., Kamdem, A., Vasile, M., Kasbi, F., & Pondarré, C. (2015). Chronic and acute anemia and extracranial internal carotid stenosis are risk factors for silent cerebral infarcts in sickle cell anemia. Blood, 125(10), 1653–1661.CrossRefGoogle ScholarPubMed
Bills, S.E., Johnston, J.D., Shi, D., & Bradshaw, J. (2021). Social-environmental moderators of neurodevelopmental outcomes in youth born preterm: A systematic review. Child Neuropsychology, 27(3), 351–370.CrossRefGoogle ScholarPubMed
Blencowe, H., Cousens, S., Chou, D., Oestergaard, M., Say, L., Moller, A.-B. …, The Born Too Soon Preterm Birth Action Group (see acknowledgement for full list). (2013). Born Too Soon: The global epidemiology of 15 million preterm births. Reproductive Health, 10(1), S2.CrossRefGoogle ScholarPubMed
Boardman, J. & Counsell, S. (2020). Invited review: Factors associated with atypical brain development in preterm infants: Insights from magnetic resonance imaging. Neuropathology and Applied Neurobiology, 46(5), 413–421.CrossRefGoogle ScholarPubMed
Böhm, B., Smedler, A., & Forssberg, H. (2004). Impulse control, working memory and other executive functions in preterm children when starting school. Acta Paediatrica, 93(10), 1363–1371.CrossRefGoogle ScholarPubMed
Brayette, M., Saliba, E., Malvy, J., Blanc, R., Ponson, L., Tripi, G. …, & Bonnet-Brilhault, F. (2019). Incomplete gestation has an impact on cognitive abilities in autism spectrum disorder. Journal of Autism and Developmental Disorders, 49(10), 4339–4345.CrossRefGoogle ScholarPubMed
Breeman, L.D., Jaekel, J., Baumann, N., Bartmann, P., & Wolke, D. (2016). Attention problems in very preterm children from childhood to adulthood: The Bavarian Longitudinal Study. Journal of Child Psychology and Psychiatry, 57(2), 132–140.CrossRefGoogle ScholarPubMed
Breeman, L.D., Jaekel, J., Baumann, N., Bartmann, P., & Wolke, D. (2015). Preterm cognitive function into adulthood. Pediatrics, 136(3), 415–423.CrossRefGoogle ScholarPubMed
Brousseau, D.C., Owens, P.L., Mosso, A.L., Panepinto, J.A., & Steiner, C.A. (2010). Acute care utilization and rehospitalizations for sickle cell disease. Journal of the American Medical Association, 303(13), 1288–1294.CrossRefGoogle ScholarPubMed
Brown, R.T., Buchanan, I., Doepke, K., Eckman, J.R., Baldwin, K., Goonan, B., & Schoenherr, S. (1993). Cognitive and academic functioning in children with sickle-cell disease. Journal of Clinical Child Psychology, 22(2), 207–218.CrossRefGoogle Scholar
Brown, R.T., Davis, P.C., Lambert, R., Hsu, L., Hopkins, K., & Eckman, J. (2000). Neurocognitive functioning and magnetic resonance imaging in children with sickle cell disease. Journal of Pediatric Psychology, 25(7), 503–513.CrossRefGoogle ScholarPubMed
Brydges, C.R., Landes, J.K., Reid, C.L., Campbell, C., French, N., & Anderson, M. (2018). Cognitive outcomes in children and adolescents born very preterm: A meta-analysis. Developmental Medicine & Child Neurology, 60(5), 452–468.CrossRefGoogle ScholarPubMed
Choi, S., O’Neil, S.H., Joshi, A.A., Li, J., Bush, A.M., Coates, T.D., … Wood, J.C. (2019). Anemia predicts lower white matter volume and cognitive performance in sickle and non-sickle cell anemia syndrome. American Journal of Hematology, 94(10), 1055–1065.CrossRefGoogle ScholarPubMed
Colombatti, R., Ermani, M., Rampazzo, P., Manara, R., Montanaro, M., Basso, G., … Sainati, L. (2015). Cognitive evoked potentials and neural networks are abnormal in children with sickle cell disease and not related to the degree of anaemia, pain and silent infarcts. British Journal of Haematology, 169(4), 597–600.CrossRefGoogle ScholarPubMed
Colombatti, R., Lucchetta, M., Montanaro, M., Rampazzo, P., Ermani, M., Talenti, G., … Sainati, L. (2016). Cognition and the default mode network in children with sickle cell disease: a resting state functional MRI study. PloS One, 11(6), 1–13.CrossRefGoogle ScholarPubMed
Counsell, S.J., Edwards, A.D., Chew, A.T., Anjari, M., Dyet, L.E., Srinivasan, L. … Rutherford, M.A. (2008). Specific relations between neurodevelopmental abilities and white matter microstructure in children born preterm. Brain, 131(12), 3201–3208.CrossRefGoogle ScholarPubMed
DeBaun, M.R., Armstrong, F.D., McKinstry, R.C., Ware, R.E., Vichinsky, E., & Kirkham, F.J. (2012). Silent cerebral infarcts: A review on a prevalent and progressive cause of neurologic injury in sickle cell anemia. Blood, 119(20), 4587–4596.CrossRefGoogle ScholarPubMed
DeBaun, M.R., Schatz, J., Siegel, M., Koby, M., Craft, S., Resar, L. … Lee, R. (1998). Cognitive screening examinations for silent cerebral infarcts in sickle cell disease. Neurology, 50(6), 1678–1682.CrossRefGoogle ScholarPubMed
Dimitrova, R., Pietsch, M., Christiaens, D., Ciarrusta, J., Wolfers, T., Batalle, D. … Price, A.N. (2020). Heterogeneity in brain microstructural development following preterm birth. Cerebral Cortex, 30(9), 4800–4810.CrossRefGoogle ScholarPubMed
Donders, J. & Kim, E. (2019). Effect of cognitive reserve on children with traumatic brain injury. Journal of the International Neuropsychological Society: JINS, 25(4), 355–361.CrossRefGoogle ScholarPubMed
Edwards, C.L., Scales, M.T., Loughlin, C., Bennett, G.G., Harris-Peterson, S., De Castro, L.M. … Johnson, S. (2005). A brief review of the pathophysiology, associated pain, and psychosocial issues in sickle cell disease. International Journal of Behavioral Medicine, 12(3), 171–179.CrossRefGoogle ScholarPubMed
Epping, A.S., Myrvik, M.P., Newby, R.F., Panepinto, J.A., Brandow, A.M., & Scott, J.P. (2013). Academic attainment findings in children with sickle cell disease. Journal of School Health, 83(8), 548–553.CrossRefGoogle ScholarPubMed
Fay, T.B., Yeates, K.O., Taylor, H.G., Bangert, B., Dietrich, A., Nuss, K.E. … Wright, M. (2010). Cognitive reserve as a moderator of postconcussive symptoms in children with complicated and uncomplicated mild traumatic brain injury. Journal of the International Neuropsychological Society: JINS, 16(1), 94–105.CrossRefGoogle ScholarPubMed
Fidan, E., Lewis, J., Kline, A.E., Garman, R.H., Alexander, H., Cheng, J.P. … Kochanek, P.M. (2016). Repetitive mild traumatic brain injury in the developing brain: Effects on long-term functional outcome and neuropathology. Journal of Neurotrauma, 33(7), 641–651.CrossRefGoogle ScholarPubMed
Ford, A.L., Ragan, D.K., Fellah, S., Binkley, M.M., Fields, M.E., Guilliams, K.P. … Lee, J.-M. (2018). Silent infarcts in sickle cell disease occur in the border zone region and are associated with low cerebral blood flow. Blood, 132(16), 1714–1723.CrossRefGoogle ScholarPubMed
Guarini, A., Bonifacci, P., Tobia, V., Alessandroni, R., Faldella, G., & Sansavini, A. (2019). The profile of very preterm children on academic achievement. A cross-population comparison with children with specific learning disorders. Research in Developmental Disabilities, 87(8709782, rid), 54–63.CrossRefGoogle ScholarPubMed
Hijmans, C.T., Fijnvandraat, K., Grootenhuis, M.A., van Geloven, N., Heijboer, H., Peters, M., & Oosterlaan, J. (2010). Neurocognitive deficits in children with sickle cell disease: A comprehensive profile. Pediatric Blood & Cancer, 56(5), 783–788.CrossRefGoogle ScholarPubMed
Hogan, A.M., Kirkham, F.J., Prengler, M., Telfer, P., Lane, R., Vargha-Khadem, F., & de Haan, M. (2006). An exploratory study of physiological correlates of neurodevelopmental delay in infants with sickle cell anaemia. British Journal of Haematology, 132(1), 99–107.CrossRefGoogle ScholarPubMed
Karkoska, K.A., Haber, K., Elam, M., Strong, S., & McGann, P.T. (2021). Academic challenges and school service utilization in children with sickle cell disease. The Journal of Pediatrics, 230, 182–190.CrossRefGoogle ScholarPubMed
Kawadler, J.M., Clayden, J.D., Kirkham, F.J., Cox, T.C., Saunders, D.E., & Clark, C.A. (2013). Subcortical and cerebellar volumetric deficits in paediatric sickle cell anaemia. British Journal of Haematology, 163(3), 373–376.CrossRefGoogle ScholarPubMed
Kim, J.A., Leung, J., Lerch, J.P., & Kassner, A. (2016). Reduced cerebrovascular reserve is regionally associated with cortical thickness reductions in children with sickle cell disease. Brain Research, 1642, 263–269.CrossRefGoogle ScholarPubMed
Lundequist, A., Böhm, B., & Smedler, A.-C. (2013). Individual neuropsychological profiles at age 5½ years in children born preterm in relation to medical risk factors. Child Neuropsychology, 19(3), 313–331.CrossRefGoogle ScholarPubMed
Manara, R., Dalla Torre, A., Lucchetta, M., Ermani, M., Favaro, A., Baracchini, C., … Colombatti, R. (2021). Visual cortex changes in children with sickle cell disease and normal visual acuity: a multimodal magnetic resonance imaging study. British Journal of Haematology, 192(1), 151–157.CrossRefGoogle ScholarPubMed
Manara, R., Talenti, G., Rampazzo, P., Ermani, M., Montanaro, M., Baracchini, C., … Colombatti, R. (2017). Longitudinal evaluation of cerebral white matter hyperintensities lesion volume in children with sickle cell disease. British Journal of Haematology, 176(3), 485–487.CrossRefGoogle ScholarPubMed
Miller, S.T., Macklin, E.A., Pegelow, C.H., Kinney, T.R., Sleeper, L.A., Bello, J.A., … Cooperative Study of Sickle Cell Disease. (2001). Silent infarction as a risk factor for overt stroke in children with sickle cell anemia: A report from the Cooperative Study of Sickle Cell Disease. The Journal of Pediatrics, 139(3), 385–390.CrossRefGoogle ScholarPubMed
Newcomer, P.L. & Hammill, D.D. (1997). Test of Language Development-Primary, Third Edition. Austin, TX: PRO-ED.Google Scholar
Nur, E., Kim, Y.S., Truijen, J., van Beers, E.J., Davis, S.C., Brandjes, D.P., … van Lieshout, J.J. (2009). Cerebrovascular reserve capacity is impaired in patients with sickle cell disease. Blood, The Journal of the American Society of Hematology, 114(16), 3473–3478.Google ScholarPubMed
Piel, F.B., Steinberg, M.H., & Rees, D.C. (2017). Sickle cell disease. New England Journal of Medicine, 376(16), 1561–1573.CrossRefGoogle ScholarPubMed
Pegelow, C.H., Macklin, E.A., Moser, F.G., Wang, W.C., Bello, J.A., Miller, S.T. … Zimmerman, R.A. (2002). Longitudinal changes in brain magnetic resonance imaging findings in children with sickle cell disease. Blood, The Journal of the American Society of Hematology, 99(8), 3014–3018.Google ScholarPubMed
Pegelow, C.H., Wang, W., Granger, S., Hsu, L.L., Vichinsky, E., Moser, F.G., … Brambilla, D. (2001). Silent infarcts in children with sickle cell anemia and abnormal cerebral artery velocity. Archives of Neurology, 58(12), 2017–2021.CrossRefGoogle ScholarPubMed
Powars, D., Wilson, B., Imbus, C., Pegelow, C., & Allen, J. (1978). The natural history of stroke in sickle cell disease. The American Journal of Medicine, 65(3), 461–471.CrossRefGoogle ScholarPubMed
Prengler, M., Pavlakis, S.G., Prohovnik, I., & Adams, R.J. (2002). Sickle cell disease: The neurological complications. Annals of Neurology, 51(5), 543–552.CrossRefGoogle ScholarPubMed
Prussien, K.V., Jordan, L.C., DeBaun, M.R., & Compas, B.E. (2019). Cognitive function in sickle cell disease across domains, cerebral infarct status, and the lifespan: a meta-analysis. Journal of Pediatric Psychology, 44(8), 948–958.CrossRefGoogle ScholarPubMed
Prussien, K.V., Siciliano, R.E., Ciriegio, A.E., Anderson, A.S., Sathanayagam, R., DeBaun, M.R. … Compas, B.E. (2020). Correlates of cognitive function in sickle cell disease: A meta-analysis. Journal of Pediatric Psychology, 45(2), 145–155.CrossRefGoogle ScholarPubMed
Rabie, N., Bird, T., Magann, E., Hall, R., & McKelvey, S. (2015). ADHD and developmental speech/language disorders in late preterm, early term and term infants. Journal of Perinatology, 35(8), 660–664.CrossRefGoogle ScholarPubMed
Sanchez, C.E., Schatz, J., & Roberts, C.W. (2010). Cerebral blood flow velocity and language functioning in pediatric sickle cell disease. Journal of the International Neuropsychological Society: JINS, 16(2), 326.CrossRefGoogle ScholarPubMed
Sansavini, A., Guarini, A., & Caselli, M.C. (2011). Preterm birth: Neuropsychological profiles and atypical developmental pathways. Developmental Disabilities Research Reviews, 17(2), 102–113.CrossRefGoogle ScholarPubMed
Schatz, J., Brown, R.T., Pascual, J., Hsu, L., & DeBaun, M. (2001). Poor school and cognitive functioning with silent cerebral infarcts and sickle cell disease. Neurology, 56(8), 1109–1111.CrossRefGoogle ScholarPubMed
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, 27(8), 739–748.CrossRefGoogle ScholarPubMed
Schatz, J., Finke, R., & Roberts, C.W. (2004). Interactions of biomedical and environmental risk factors for cognitive development: A preliminary study of sickle cell disease. Journal of Developmental & Behavioral Pediatrics, 25(5), 303–310.CrossRefGoogle ScholarPubMed
Schatz, J., Puffer, E.S., Sanchez, C., Stancil, M., & Roberts, C.W. (2009). Language processing deficits in sickle cell disease in young school-age children. Developmental Neuropsychology, 34(1), 122–136.CrossRefGoogle ScholarPubMed
Sherlock, R.L., Anderson, P.J., Doyle, L.W., & Victorian Infant Collaborative Study Group. (2005). Neurodevelopmental sequelae of intraventricular haemorrhage at 8 years of age in a regional cohort of ELBW/very preterm infants. Early Human Development, 81(11), 909–916.CrossRefGoogle Scholar
Stålnacke, J., Lundequist, A., Böhm, B., Forssberg, H., & Smedler, A.-C. (2015). Individual cognitive patterns and developmental trajectories after preterm birth. Child Neuropsychology, 21(5), 648–667.CrossRefGoogle ScholarPubMed
Stern, Y. (2017). An approach to studying the neural correlates of reserve. Brain Imaging and Behavior, 11(2), 410–416.CrossRefGoogle ScholarPubMed
Sundd, P., Gladwin, M.T., & Novelli, E.M. (2019). Pathophysiology of sickle cell disease. Annual Review of Pathology: Mechanisms of Disease, 14, 263–292.CrossRefGoogle ScholarPubMed
Taylor, H.G., Klein, N., Anselmo, M.G., Minich, N., Espy, K.A., & Hack, M. (2011). Learning problems in kindergarten students with extremely preterm birth. Archives of Pediatrics & Adolescent Medicine, 165(9), 819–825.CrossRefGoogle ScholarPubMed
Vandewouw, M.M., Young, J.M., Mossad, S.I., Sato, J., Whyte, H.A., Shroff, M.M., & Taylor, M.J. (2019). Mapping the neuroanatomical impact of very preterm birth across childhood. Human Brain Mapping, 41, 892–905.CrossRefGoogle ScholarPubMed
Verduzco, L.A. & Nathan, D.G. (2009). Sickle cell disease and stroke. Blood, 114(25), 5117–5125.CrossRefGoogle ScholarPubMed
Vohr, B.R., Allan, W., Katz, K.H., Schneider, K., Tucker, R., & Ment, L.R. (2014). Adolescents born prematurely with isolated grade 2 haemorrhage in the early 1990s face increased risks of learning challenges. Acta Paediatrica, 103(10), 1066–1071.CrossRefGoogle ScholarPubMed
Volpe, J.J. (2019). Dysmaturation of premature brain: Importance, cellular mechanisms, and potential interventions. Pediatric Neurology, 95, 42–66.CrossRefGoogle ScholarPubMed
Vynorius, K.C., Paquin, A.M., & Seichepine, D.R. (2016). Lifetime multiple mild traumatic brain injuries are associated with cognitive and mood symptoms in young healthy college students. Frontiers in Neurology, 7, 188.CrossRefGoogle ScholarPubMed
Wang, W.C., Pavlakis, S.G., Helton, K.J., McKinstry, R.C., Casella, J.F., Adams, R.J., & Rees, R.C. (2008). MRI abnormalities of the brain in one-year-old children with sickle cell anemia. Pediatric Blood & Cancer, 51(5), 643–646.CrossRefGoogle ScholarPubMed
Whiteman, V., Salinas, A., Weldeselasse, H.E., August, E.M., Mbah, A.K., Aliyu, M.H., & Salihu, H.M. (2013). Impact of sickle cell disease and thalassemias in infants on birth outcomes. European Journal of Obstetrics & Gynecology and Reproductive Biology, 170(2), 324–328.CrossRefGoogle ScholarPubMed
Wong, H.S. & Edwards, P. (2013). Nature or nurture: A systematic review of the effect of socio-economic status on the developmental and cognitive outcomes of children born preterm. Maternal and Child Health Journal, 17(9), 1689–1700.CrossRefGoogle ScholarPubMed
Woodcock, R., McGrew, K.S., & Mather, N. (2001). Technical Manual. Woodcock-Johnson III.Google Scholar
Yarboi, J., Compas, B.E., Brody, G.H., White, D., Rees Patterson, J., Ziara, K., & King, A. (2017). Association of social-environmental factors with cognitive function in children with sickle cell disease. Child Neuropsychology, 23(3), 343–360.CrossRefGoogle ScholarPubMed
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