NEUROPSYCHOLOGICAL AND BEHAVIORAL OUTCOMES FROM A COMPREHENSIVE MAGNETIC RESONANCE STUDY OF CHILDREN WITH FETAL ALCOHOL SPECTRUM DISORDERS
Main Article Content
Keywords
Fetal alcohol spectrum disorder (FASD), magnetic resonance (MR), FASD 4-Digit Diagnostic Code, neuropsychological
Abstract
Background
Clinical and research advancements in the field of fetal alcohol spectrum disorders (FASD) require accurate and valid identification of FASD clinical subgroups.
Objectives
A comprehensive neuropsychological battery, coupled with magnetic resonance imaging, (MRI), MR spectroscopy (MRS), and functional MRI (fMRI) were administered to children with fetal alcohol spectrum disorders (FASD) to determine if global and/or focal abnormalities could be identified across the spectrum, and distinguish diagnostic subclassifications within the spectrum. The neuropsychological outcomes of the comprehensive neuroimaging study are presented here.
Methods
The study groups included: 1) FAS/Partial FAS; 2) Static Encephalopathy/Alcohol Exposed (SE/AE); 3) Neurobehavioral Disorder/Alcohol Exposed (ND/AE) as diagnosed by an interdisciplinary team using the FASD 4-Digit Code; and 4) healthy peers with no prenatal alcohol. A standardized neuropsychological battery was administered to each child and their primary caregiver by a psychologist.
Results
Use of the 4-Digit Code produced three clinically and statistically distinct FASD clinical subgroups. The three subgroups (ND/AE, SE/AE and FAS/PFAS) reflected a linear continuum of increasing neuropsychological impairment and physical abnormality, representing the full continuum of FASD. Behavioral and psychiatric disorders were comparably prevalent across the three FASD groups, and significantly more prevalent than among the Controls. All three FASD subgroups had comparably high levels of prenatal alcohol exposure.
Conclusions
Although ND/AE, SE/AE, and FAS/PFAS are distinct FASD subgroups, these groups are not distinguishable solely by their neuropsychological profiles. While all children within a group shared the same magnitude of neuropsychological impairment, the patterns of impairment showed considerable individual variability. MRI, MRS and fMRI further distinguished these FASD subgroups.
References
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21. Streissguth AP, Aase JM, Clarren SK, Randels SP, LaDue RA, Smith DF. Fetal alcohol syndrome in adolescents and adults. Journal of the American Medical Association. 1991;265:1961-1967.
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30. Fryer SL, Tapert SF, Mattson SN, Paulus MP, Spadoni AD, Riley EP. Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcohol Clin Exp Res. 2007;31(1-10):1.
31. Astley SJ, Clarren SK. Diagnosing the full spectrum of fetal alcohol exposed individuals: Introducing the 4-Digit Diagnostic Code. Alcohol Alcohol. 2000;35:400-410.
32. Hoyme HE, May PA, Kalberg WO, et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 Institute of Medicine criteria. Pediatrics. 2005;115:39-47.
33. Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods. New York: Van Nostrand Reinhold Company; 1982.
34. Astley SJ, Clarren SK. A case definition and photographic screening tool for the facial phenotype of fetal alcohol syndrome. J Pediatr. 1996;129:33-41.
35. Astley SJ. Fetal Alcohol Syndrome Facial Photograph Analysis Software. In: Astley SJ, editor. 1.0 ed. Seattle: University of Washington; 2003.
36. Mattson SN, Riley EP. A review of neurobehavioral deficits in children with FAS or prenatal exposure to alcohol. Alcohol Clin Exp Res. 1998;22:279-294.
37. Connor PD, Streissguth AP, Sampson PD, Bookstein FL, Barr HM. Individual differences in auditory and visual attention among fetal alcohol-affected adults. Alcohol Clin Exp Res. 1999;23:1395-1402.
38. Olson HC, Jirikowic T, Kartin D, Astley SJ. Responding to the challenge of early intervention for fetal alcohol spectrum disorders. Infants and Young Children. 2007;20:172-189.
39. Roebuck TM, Mattson SN, Riley EP. Behavioral and psychosocial profiles of alcohol-exposed children. Alcohol Clin Exp Res. 1999;23:1070-1076.
40. Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiol Community Health. 1990;1(1):43-46.
41. Bender R, Lange S. Adjusting for multiple testing--when and how? J Clin Epidemiol. 2001;54(4):343-349.
42. Riley EP, Mattson SN, Sowell ER, Jernigan TL, Sobel DF, Jones KL. Abnormalities of the corpus callosum in children prenatally exposed to alcohol Alcohol Clin Exp Res. 1995;19:1198-1202.
43. Jeret JS, Serur D, Wisniewski K, Fisch C. Frequency of agenesis of the corpus callosum in the developmentally disabled population as determined by computerized tomography. Pediatr Neurosci. 1986;12:101-103.
44. Sowell E, Johnson A, Kan E, et al. Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. Journal of Neuroscience. 2008;28(6):1313-1319.
45. Haier R, Jung R, Yeo R, Head K, Alkire M. Structural brain variation and general intelligence. Neuroimage. 2004;23:425-433.
46. Waber DP, Moor CD, Forbes PW, et al. 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. J Int Neuropsychol Soc. 2007;13:1-18.
47. Niccols A. Fetal alcohol syndrome and the developing socio-emotional brain. Brain Cogn. 2007;65:135-142.
48. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL. Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology. 1998;12(1):146-153.
49. Conry J. Neuropsychological deficits in fetal alcohol syndrome and fetal alcohol effects. Alcohol Clin Exp Res. 1990;14(5):650-655.
50. Moore KL, Persaud TVN, Shiota K. Color Atlas of Clinical Embryology. Philidelphia, PA: W B Saunders Co; 1994.
51. Whaley SE, O'Connor MJ, Gunderson B. Comparison of the adaptive functioning of children prenatally exposed to alcohol to a nonexposed clinical sample. Alcohol Clin Exp Res. 2001;25:1018-1024.
52. Mutti M, Sterling HM, Spalding N. Quick Neurological Screen Test. Novato, CA: Academic Therapy Publications; 1978.
53. Wechsler D. WISC-III Manual. San Antonio TX; The Psychological Corporation 1996.
54. Wilkinson GS. The Wide Range Achievement Test 3. 3rd ed. Wilmington, Delaware: Wide Range Inc; 1994.
55. Huebner FS. Review of KeyMath-Revised. Journal of Psychoeducational Assessment. 1989;7:364-367.
56. Beery KE. The Beery-Buktenica developmental test of visual-motor integration. 4th ed. Parsippany, NJ: Modern Curriculum Press; 1997.
57. Spreen O, Strauss E. A compendium of neuropsychological tests: Administration norms and commentary. 2nd ed. New York NY: Oxford University Press; 1998.
58. Delis DC, Kaplan E, Kramer JH, Ober BA. Delis-Kaplan Executive Function Scale. San Antonio, TX: The Psychological Corporation; 2000.
59. Heaton R, Chelune GJ, Talley JL, Kay GG, Curtiss G. Wisconsin Card Sorting Test. Manual Revised and Expanded. Odessa, FL: Psychological Assessment Resources; 1993.
60. Delis DC, Kramer JH, Kaplan E, Ober BA. CVLT-C: California Verbal Learning Test— Children’s Version. San Antonio, TX: Psychological Corporation; 1994.
61. Tinius TP. The Integrated Visual and Auditory Continuous Performance Test as a Neuropsychological Measure. Archives of Clinical Neuropsychology. 2003;18:439-454.
62. Newcomer P, Hammill DD. Using the test of language development with language-impaired children. J Learn Disabil. 1978;11:521-524.
63. Wiig EH, Secord W. Test of Language Competence-Expanded Edition. The Psychological Corporation; 1988.
64. Wiig EH, Secord W. Test of Word Knowledge San Antonio, TX: The Psychological Corporation; 1992.
65. Sparrow SS, Balla DA, Cicchetti DV. Vineland Adaptive Behavior Scales: Interview Edition Survey Form Manual Circle Pines, MN: American Guidance Service; 1984.
66. Achenbach T. Child Behavior Checklist (CBCL 6-18) Burlington: University Associates in Psychiatry; 2001.
67. Gioia GA, Isquith PK, Guy SC, Kenworth L. Behavior rating inventory of executive function (BRIEF). Odessa, FL: Psychological Assessment Resources; 2000.
68. Shaffer D, Fischer P, Lucas C, Comer J. Diagnostic Interview for Children (DISC-V). New York: Columbia University; 2003.
2. Astley SJ, Aylward EH, Olson HC, et al. Functional magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Journal of Neurodevelopmental Disorders. 2009.
3. Astley SJ. Diagnostic Guide for Fetal Alcohol Spectrum Disorders: The 4-Digit Diagnostic Code. 3rd ed. Seattle WA: University of Washington Publication Services; 2004.
4. Smith DW. The fetal alcohol syndrome. Hosp Pract. 1979;14(10):121-128.
5. Bertrand J, Floyd RL, Weber MK, et al. National Task Force on FAS/FAE Fetal Alcohol Syndrome: Guidelines for Referral and Diagnosis: Atlanta GA: Centers for Disease Control and Prevention 2004.
6. Chudley AE, Conroy J, Cook JL, Loock C, Rosales T, LeBlanc N. Public Health Agency of Canada’s National Advisory Committee on Fetal Alcohol Spectrum Disorder. Canadian guidelines for diagnosis. Can Med Assoc J. 2005;172:S1-S21.
7. Astley SJ, Clarren SK. Measuring the facial phenotype of individuals with prenatal alcohol exposure: correlations with brain dysfunction. Alcohol Alcohol. 2001;36:147-159.
8. Astley S, Stachowiak J, Clarren S, Clausen C. Application of the fetal alcohol syndrome facial photographic screening tool in a foster care population. J Pediatr. 2002;141(5):712-717.
9. Aase JM, Jones KL, Clarren SK. Do we need the term “FAE”? Pediatrics. 1995;95:428-430.
10. Streissguth AP, Bookstein FL, Sampson PC, Barr HM. The enduring effects of prenatal alcohol exposure on child development: Birth through seven years a partial least squares solution. Ann Arbor MI: University of Michigan Press; 1993.
11. Stratton K, Howe C, Battaglia F. Fetal Alcohol Syndrome: Diagnosis Epidemiology Prevention and Treatment. Institute of Medicine. Washington D C National Academy Press; 1996.
12. Streissguth AP, Bookstein FL, Barr HM, Sampson PD, O'Malley K, Young JK. Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. J Dev Behav Pediatr. 2004;25(4):228-238.
13. Kerns KA, Don A, Mateer CA, Streissguth AP. Cognitive deficits in nonretarded adults with fetal alcohol syndrome. J Learn Disabil. 1997;30:685-693.
14. McGee CL, Sconfeld AM, Roebuck-Spencer TM, Riley EP, Mattson SN. Children with heavy prenatal alcohol exposure demonstrate deficits on multiple measures of concept formation. Alcohol Clin Exp Res. 2008;32(8).
15. Rasmussen C. Executive functioning and working memory in fetal alcohol spectrum disorder. Alcohol Clin Exp Res. 2005;29:1359- 1367.
16. Rasmussen C, Horne K, Witol A. Neurobehavioral functioning in children with fetal alcohol spectrum disorder. Child Neuropsychology. 2006;12(6):453-468.
17. Connor PD, Sampson PD, Bookstein FL, Barr HM, Streissguth AP. Direct and indirect effects of prenatal alcohol damage on executive function. Developmental Neuropsychology. 2000;18:331-354.
18. Mattson SN, Schoenfeld AM, Riley EP. Teratogenic effects of alcohol on brain and behavior. Alcohol Research & Health. 2001;25:185-191.
19. Church M, Kaltenbach J. Hearing, speech, language, and vestibular disorders in the fetal alcohol syndrome: A literature review. Alcohol Clin Exp Res. 1997;21(3):495-512.
20. Franklin L, Dietz J, Jirikowic T, Astley S. Children with fetal alcohol spectrum disorders: Problem behaviors and sensory processing. Am J Occup Ther. 2008;62:265-273.
21. Streissguth AP, Aase JM, Clarren SK, Randels SP, LaDue RA, Smith DF. Fetal alcohol syndrome in adolescents and adults. Journal of the American Medical Association. 1991;265:1961-1967.
22. Thomas S, Kelly S, Mattson S, Riley E. Comparison of social abilities of children with FAS to those of children with similar IQ scores and normal controls. Alcohol Clin Exp Res. 1998;22:528-533.
23. Kodituwakku PW. Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: a review. Neurosci Biobehav Rev. 2007;31(2):192-201.
24. Archibald SL, Fennema-Notestine C, Ganst A, Riley EP, Mattson SN, Jernigan TL. Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol. 2001;43:148-154.
25. Mattson SN, Riley EP, Sowell ER, Jernigan TL, Sobel DF, Jones KL. A decrease in the size of the basal ganglia in children with FAS. Alcohol Clin Exp Res. 1996;20:1088-1093.
26. Sowell ER, Thompson PM, Mattson SN, et al. Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport. 2001;12:515- 523.
27. Bookstein FL, Sampson PD, Connor PD, Streissguth AP. Midline corpus callosum is a neuroanatomical focus of fetal alcohol damage. Anat Rec. 2002;269:162-174.
28. Malisza KL, Allman A, Shiloff D, Jakobson L, Longstaffe S, Chudley AE. Evaluation of spatial working memory function in children and adults with fetal alcohol spectrum disorders: A functional magnetic resonance imaging study. Pediatr Res. 2005;58:1150- 1157.
29. Sowell ER, Lu LH, O'Hare ED, et al. Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure Neuroreport. 2007;18:636- 639.
30. Fryer SL, Tapert SF, Mattson SN, Paulus MP, Spadoni AD, Riley EP. Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcohol Clin Exp Res. 2007;31(1-10):1.
31. Astley SJ, Clarren SK. Diagnosing the full spectrum of fetal alcohol exposed individuals: Introducing the 4-Digit Diagnostic Code. Alcohol Alcohol. 2000;35:400-410.
32. Hoyme HE, May PA, Kalberg WO, et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 Institute of Medicine criteria. Pediatrics. 2005;115:39-47.
33. Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods. New York: Van Nostrand Reinhold Company; 1982.
34. Astley SJ, Clarren SK. A case definition and photographic screening tool for the facial phenotype of fetal alcohol syndrome. J Pediatr. 1996;129:33-41.
35. Astley SJ. Fetal Alcohol Syndrome Facial Photograph Analysis Software. In: Astley SJ, editor. 1.0 ed. Seattle: University of Washington; 2003.
36. Mattson SN, Riley EP. A review of neurobehavioral deficits in children with FAS or prenatal exposure to alcohol. Alcohol Clin Exp Res. 1998;22:279-294.
37. Connor PD, Streissguth AP, Sampson PD, Bookstein FL, Barr HM. Individual differences in auditory and visual attention among fetal alcohol-affected adults. Alcohol Clin Exp Res. 1999;23:1395-1402.
38. Olson HC, Jirikowic T, Kartin D, Astley SJ. Responding to the challenge of early intervention for fetal alcohol spectrum disorders. Infants and Young Children. 2007;20:172-189.
39. Roebuck TM, Mattson SN, Riley EP. Behavioral and psychosocial profiles of alcohol-exposed children. Alcohol Clin Exp Res. 1999;23:1070-1076.
40. Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiol Community Health. 1990;1(1):43-46.
41. Bender R, Lange S. Adjusting for multiple testing--when and how? J Clin Epidemiol. 2001;54(4):343-349.
42. Riley EP, Mattson SN, Sowell ER, Jernigan TL, Sobel DF, Jones KL. Abnormalities of the corpus callosum in children prenatally exposed to alcohol Alcohol Clin Exp Res. 1995;19:1198-1202.
43. Jeret JS, Serur D, Wisniewski K, Fisch C. Frequency of agenesis of the corpus callosum in the developmentally disabled population as determined by computerized tomography. Pediatr Neurosci. 1986;12:101-103.
44. Sowell E, Johnson A, Kan E, et al. Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. Journal of Neuroscience. 2008;28(6):1313-1319.
45. Haier R, Jung R, Yeo R, Head K, Alkire M. Structural brain variation and general intelligence. Neuroimage. 2004;23:425-433.
46. Waber DP, Moor CD, Forbes PW, et al. 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. J Int Neuropsychol Soc. 2007;13:1-18.
47. Niccols A. Fetal alcohol syndrome and the developing socio-emotional brain. Brain Cogn. 2007;65:135-142.
48. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL. Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology. 1998;12(1):146-153.
49. Conry J. Neuropsychological deficits in fetal alcohol syndrome and fetal alcohol effects. Alcohol Clin Exp Res. 1990;14(5):650-655.
50. Moore KL, Persaud TVN, Shiota K. Color Atlas of Clinical Embryology. Philidelphia, PA: W B Saunders Co; 1994.
51. Whaley SE, O'Connor MJ, Gunderson B. Comparison of the adaptive functioning of children prenatally exposed to alcohol to a nonexposed clinical sample. Alcohol Clin Exp Res. 2001;25:1018-1024.
52. Mutti M, Sterling HM, Spalding N. Quick Neurological Screen Test. Novato, CA: Academic Therapy Publications; 1978.
53. Wechsler D. WISC-III Manual. San Antonio TX; The Psychological Corporation 1996.
54. Wilkinson GS. The Wide Range Achievement Test 3. 3rd ed. Wilmington, Delaware: Wide Range Inc; 1994.
55. Huebner FS. Review of KeyMath-Revised. Journal of Psychoeducational Assessment. 1989;7:364-367.
56. Beery KE. The Beery-Buktenica developmental test of visual-motor integration. 4th ed. Parsippany, NJ: Modern Curriculum Press; 1997.
57. Spreen O, Strauss E. A compendium of neuropsychological tests: Administration norms and commentary. 2nd ed. New York NY: Oxford University Press; 1998.
58. Delis DC, Kaplan E, Kramer JH, Ober BA. Delis-Kaplan Executive Function Scale. San Antonio, TX: The Psychological Corporation; 2000.
59. Heaton R, Chelune GJ, Talley JL, Kay GG, Curtiss G. Wisconsin Card Sorting Test. Manual Revised and Expanded. Odessa, FL: Psychological Assessment Resources; 1993.
60. Delis DC, Kramer JH, Kaplan E, Ober BA. CVLT-C: California Verbal Learning Test— Children’s Version. San Antonio, TX: Psychological Corporation; 1994.
61. Tinius TP. The Integrated Visual and Auditory Continuous Performance Test as a Neuropsychological Measure. Archives of Clinical Neuropsychology. 2003;18:439-454.
62. Newcomer P, Hammill DD. Using the test of language development with language-impaired children. J Learn Disabil. 1978;11:521-524.
63. Wiig EH, Secord W. Test of Language Competence-Expanded Edition. The Psychological Corporation; 1988.
64. Wiig EH, Secord W. Test of Word Knowledge San Antonio, TX: The Psychological Corporation; 1992.
65. Sparrow SS, Balla DA, Cicchetti DV. Vineland Adaptive Behavior Scales: Interview Edition Survey Form Manual Circle Pines, MN: American Guidance Service; 1984.
66. Achenbach T. Child Behavior Checklist (CBCL 6-18) Burlington: University Associates in Psychiatry; 2001.
67. Gioia GA, Isquith PK, Guy SC, Kenworth L. Behavior rating inventory of executive function (BRIEF). Odessa, FL: Psychological Assessment Resources; 2000.
68. Shaffer D, Fischer P, Lucas C, Comer J. Diagnostic Interview for Children (DISC-V). New York: Columbia University; 2003.