Four-dimensional sonography in the assessment of fetal functional neurodevelopment and behavioral patterns

Ultrasound Review of Obstetrics and Gynecology

Volumn 5, Issue 2, 2005, Pages 154-168

  Salihagić Kadić, Aida ^a   Medić, Marijana ^a   Kurjak, Asim ^a   Andonotopo, Wiku ^b   Azumendi, Guillermo ^c   Hafner, Tomislav ^a   Milenković, Dragan ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b MINISTRY OF HEALTH   (Indonesia)

^c Centro Gutenberg   (Spain)

Author keywords

4D ultrasound; Behavioral patterns; Brain lesions; Fetal neurodevelopment; Fetal stress

Indexed keywords

BEHAVIOR; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN FUNCTION; BRAIN MALFORMATION; BRAIN REGION; CENTRAL NERVOUS SYSTEM; DIAGNOSTIC IMAGING; DIAGNOSTIC VALUE; EARLY DIAGNOSIS; ECHOENCEPHALOGRAPHY; ENVIRONMENTAL FACTOR; FETUS; FETUS DEVELOPMENT; FETUS MOVEMENT; GESTATIONAL AGE; HISTOGENESIS; HUMAN; NEUROANATOMY; REVIEW;

EID: 25444511778     PISSN: 14722240     EISSN: None     Source Type: Journal    
DOI: 10.1080/14722240500190640     Document Type: Review

References (104)

1. Rees S, Harding R. Brain development during fetal life: influences of the intra-uterine environment. Neursci Lett 2004;361:111-114.
2. Harrison PJ. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999;122: 593-624.
3. Fignon A, Salihagić A, Akoka S, Moraine C, Lansac L, Laurini R, Arbeille P. Twenty-day umbilical and cerebral Doppler monitoring on a growth retarded and hypoxic fetus. Eur J Obstet Gynecol Reprod Biol 1996;66:83-86.
4. Salihagić A, Fignon A, Locateli S, Lansac J, Arbeille P. New advances in understanding fetal hypoxia. In: Chervenak F, Kurjak A, editors. Fetus as a patient. New York, London: Parthenon; 1996. pp 359-378.
5. Salihagić A, Georgescus M, Perrotin F, Laurini R, Arbeille B, Fignon A, Zudenigo D, Kurjak A, Arbeille P. Daily Doppler assessment of the fetal hemodynamic response to chronic hypoxia: a five case report. Prenat Neonat Med 2000;5:35-41.
6. Arbeille P, Perrotin F, Salihagic A, et al. Hypoxic index for the prediction of abnormal fetal heart rate at delivery in chronic fetal distress. Eur J Obstet Gynecol Reprod Biol 2005; in press.
7. Stafstrom CE, Johnston D, Wehner JM, Sheppard JR. Spontaneous neural activity in fetal brain reaggregate culture. Neuroscience 1980;10:1681-1689.
8. Streit J. Regular oscillations of synaptic activity in spinal networks in vitro. J Neurophysiol 1993;70:871-878.
9. Marder E, Calabrese R. Principles of rhythmic motor pattern generation. Physiol Rev 1996;76:687-717.
10. Okado N, Kojima T. Ontogeny of the central nervous system: neurogenesis, fibre connection, synaptogenesis and myelination in the spinal cord. In: Prechtl HFR, editor. Continuity of neural function from prenatal to postnatal life, clinics in developmental medicine. London: SIMP Heinemann; 1984. pp 31-35.
11. Landmesser LT, Morris DG. The development of functional innervation in the hind limb of the chick embryo. J Physiol 1975;249:301-326.
12. De Vries JIP, Visser GHA, Prechtl HFR. Fetal motility in the first half of the pregnancy. In: Prechtl HFR, editor. Continuity of neural functions from prenatal to postnatal life. Philadelphia: Lippincott; 1984. pp 44-64.
13. Kurjak A, Vecek N, Hafner T, Bozek T, Funduk-Kurjak B, Ujevic B. Prenatal diagnosis: what does four-dimensional ultrasound add? J Perinat Med 2002; 30:57-62.
14. Joseph R. Fetal brain and cognitive development. Dev Rev 1999;20:81-98.
15. Pomeroy SL, Volpe JJ. Development of the nervous system. In: Polin RA, Fow WW, editors. Fetal and neonatal physiology. Philadelphia: Saunders; 1992. pp 1491-1509.
16. Kostovic I. Zentralenrvensystemen. In: Hinrichsen KV, editor. Humanembryologie. Berlin: Springer; 1990. pp 381-448.
17. Molliver ME, Kostovic I, Van der Loos H. The development of synapses in cerebral cortex of the human fetus. Brain Res 1973;50:403-407.
18. Kostovic I, Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 1990;274:441-470.
19. Anand KJS, Hickey PR. Pain and its effects on human fetus. N Engl J Med 1987;317:1321-1329.
20. Kostovic I, Rakic P. Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 1984; 4:25-42.
21. Kostovic I, Goldman-Rakic PS. Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 1983;219:431-447.
22. Kostovic I, Judas M, Petanjek Z, et al. Ontogenesis of goal-directed behavior: anatomo-functional considerations. Int J Psychophysiol 1995;19:85-102.
23. Kostovic I, Judas M, Rados M, Hrabac P. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 2002;12:536-544.
24. Lightman SL, Insel TR, Ingram CD. New genomic avenues in behavioral neuroendocrinology. Eur J Neurosci 2002;16: 369-372.
25. Hanganu IL, Kilb W, Luhmann HJ. Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci 2002;22:7165-7176.
26. Kostovic I. Prenatal development of nucleus basalis complex and related fibre system in man: a histochemical study. Neuroscience 1986;17:1047-1077.
27. Buhta AT, Anand KJ. Vulnerability of the developing brain. Neuronal mechanisms. Clin Perinatol 2002;29:357-372.
28. Prechtl HFR. Ultrasound studies of human fetal behaviour. Early Hum Dev 1985;12:91-98.
29. Ianniruberto A, Tajani E. Ultrasonographic study of fetal movements. Semin Perinatol 1981;4:175-181.
30. Goto S, Kato TK. Early movements are useful for estimating the gestational weeks in the first trimester of pregnancy. In: Levski RA, Morley P, editors. Ultrasound '82. Oxford New York: Pergamon; 1983. pp 577-582.
31. Okado N. Onset of synapse formation in the human spinal cord. J Comp Neurol 1981;201:211-219.
32. Okado N. Development of the human cervical spinal cord with reference to synapse formation in the motor nucleus. J Comp Neurol 1980;191:495-513.
33. Fitzgerald M. An update on current scientific knowledge London: Department of Health; 1995.
34. Pooh RK, Ogura T. Normal and abnormal fetal hand positioning and movement in early pregnancy detected by three and four-dimensional ultrasound. Ultrasound Rev Obstet Gynecol 2004;4:46-51.
35. De Vries JIP, Visser GHA, Prechtl HFR. The emergence of fetal behavior I. Qualitative aspects. Early Hum Dev 1982; 7:301-322.
36. Awoust J, Levi S. Neurological maturation of the human fetus. Ultrasound Med Biol 1983;9:583-587.
37. Inoue M, Koyanagi T, Nakahara H. Functional development of human eye-movement in utero assessed quantitatively with real-time ultrasound. Am J Obstet Gynecol 1986;155: 170-174.
38. D'Elia A, Pighetti M, Moccia G, Santangelo N. Spontaneous motor activity in normal fetus. Early Hum Dev 2001;65: 139-144.
39. Natale R, Nasello-Paterson C, Turlink R. Longitudinal measurements of fetal breathing, body movements, and heart rate accelerations, and decelerations at 24 and 32 weeks of gestation. Am J Obstet Gynecol 1985;151:256-263.
40. Eller DP, Stramm SL, Newman RB. The effect of maternal intravenous glucose administration on fetal activity. Am J Obstet Gynecol 1992;167:1071-1104.
41. Patrick J, Campbell K, Natale R, Richardson B. Patterns of gross fetal body movements over 24-hour observation intervals during the last 10 weeks of pregnancy. Am J Obstet Gynecol 1982;142:363-371.
42. Kozuma S, Baba K, Okai T, Taketani Y. Dynamic observation of the fetal face by three-dimensional ultrasound. Ultrasound Obstet Gynecol 1999;13:283-284.
43. Kurjak A, Azumendi G, Vecek N, Kupesic S, Solak M, Varga D, Chervanek F. Fetal hand movements and facial expression in normal pregnancy studied by four-dimensional sonography. J Perinat Med. 2003;31:496-508.
44. Sporns O, Edelman GM. Solving Bernstein's problem: a proposal for the development of coordinated movement by selection. Child Dev 1993;64:960-981.
45. Changeux JP. Variation and selection in neural function. Trends Neurosci 1997;20:291-293.
46. Prechtl HFR, Knol AR. Der Einfluß der Beckenendlage auf die Fußsohlenreflexe bein neugeborenen Kind. Arch Psychiatr Zeitschr Neurol 1958;196:542-553.
47. Sival DA, Prechtl HFR, Sonder GHA, Touwen BCL. The effect of intrauterine breech position on postnatal motor functions of the lower limbs. Early Hum Dev 1993;32:161-176.
48. Graca LM, Cardoso CG, Clode N, Calhaz-Jorge C. Acute effects of maternal cigarette smoking on fetal heart rate and fetal movements felt the mother. J Perinat Med 1991; 19: 385-390.
49. Katz M, Meizner I, Holcberg G, Insler V. Reduction of cessation of fetal movements after administration of steroids for enhancement of lung maturation. Isr J Med Science 1988; 24:5-9.
50. Prechtl HFR, Einspieler C. Is neurological assessment of the fetus possible? Eur J Obstet Gynecol Reprod Biol 1997; 75:81-84.
51. Einspieler C, Prechtl HF, Ferrari F, Cioni G, Boss AF. The qualitative assessment of general movements in preterm, term and young infants - review of the methodology. Early Hum Dev 1997;50;47-60.
52. Kurjak A, Pooh RK, Merce LT, Carrera JM, Salihagić-Kadić A, Andonotopo W. Structural and functional early human development assessed by three-dimensional (3D) and four-dimensional (4D) sonography. Fertil Steril 2005; in press.
53. Andonotopo W, Salihagić-Kadić A, Medic M, Milenkovic D. The assessment of embryonic and fetal neurodevelopment in early pregnancy: comparison between 2D and 4D scanning. J Perinat Med 205; submitted.
54. Kurjak A, Stanojevic M, Andonotopo W, Salihagić-Kadić A, Carrera JM, Azumendi G. Behavioral pattern continuity from prenatal to postnatal life - a study by four-dimensional (4D) ultrasonography. J Perinat Med 2004; 32:346-353.
55. Crespi EJ, Denver RJ. Ancient origins of human developmental plasticity. Am J Hum Biol 2005;17:44-54.
56. Monk C, Fifer WP, Myers MM, Sloan RP, Trien L, Hurtado A. Maternal stress responses and anxiety during pregnancy: effects on fetal heart rate. Dev Psychobiol 2000;36:67-77.
57. DiPietro JA, Hilton SC, Hawkins M, Costigan KA, Pressman EK. Maternal stress and affect influence fetal neurobehavioral development. Dev Psychol 2002;38:659-668.
58. Amiel-Tison C, Cabrol D, Denver R, Jarreau PH, Papiernik E, Piazza PV. Fetal adaptation to stress Part I: acceleration of fetal maturation and earlier birth triggered by placental insufficiency in humans. Early Hum Dev 2004;78:15-27.
59. Howe DC, Gertler A, Challis JR. The late gestation increase in circulating ACTH and cortisol in the fetal sheep is suppressed by intracerebroventricular infusion of recombinant ovine leptin. J Endocrinol 2002;174:259-266.
60. Hundertmark S, Ragosch V, Zimmermann B, Halis G, Arabin B, Witzel HK. Effect of dexamethasone, triiodothyronine and dimethyl-isopropyl-thyronine on lung maturation of the fetal rat lung. J Perinat Med 1999;27:309-315.
61. Sandman CA, Wadhwa PD, Chicz-Demet A, Chiz-DeMet A, Porto M, Garite TJ. Maternal corticortropin-releasing hormone and habituation in human fetus. Dev Psychobiol 1999;34:163-173.
62. Amiel-Tison C, Cabrol D, Denver R, Jarreau PH, Papiernik E, Piazza PV. Fetal adaptation to stress Part II. Evolutionary aspects; Stress induced hippocampal damage; long-term effects on behavior; consequences on adult health. Early Hum Dev 2004;78:81-94.
63. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000;97:11032-11037.
64. Deminiere JM, Piazza PV, Guegan G, Abrous DN, Maccari S, Le Moal M, Simon H. Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res 1992;586:135-139.
65. McEwen BS, Sapolsky RM. Stress and cognitive function. Curr Opin Neurobiol 1995;5:205-216.
66. Sapolsky RM, Krey LC, McEwen BS. The neuroendocrinology of stress and aging; the glucocorticoid cascade hypothesis. Endocr Rev 1986;7:284-301.
67. Sapolsky RM. Stress, the aging brain, and the mechanisms of neuron death. Cambridge, MA: MIT Press; 1992.
68. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NP, Thakur M, McEven BS, Haurger RL, Meaney MJ. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci 1998;1: 69-73.
69. Henry C, Guegant G, Cador M, Arnault E, Arsaut J, Le Moal M, Demotes-Mainard J. Prenatal stress in rats facilitates amphetamine induced sensitization and induces long-lasting in dopamine receptors in the nucleus accumbens. Brain Res 1995;685:179-186.
70. Koehl M, Bjijou Y, Le Moal M, Cador M. Nicotine-induced locomotor activity is increased by preexposure of rats to prenatal stress. Brain Res 2000;882:196-200.
71. Uno H, Lohmiller L, Thieme C, Kemnitz JW, Engle MJ, Roecker EB, Farrel PM. Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques: I. Hippocampus. Dev Brain Res 1990;53:157-167.
72. Barbazanges A, Piazza PV, Le Moal M, Maccari S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 1996;16:3943-3949.
73. Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N. Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Dev Neurosci 1998;16:209-216.
74. Fride E, Weinstock M. Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci 1988;42:1059-1065.
75. Fride E, Dan Y, Feldon J, Halevy G, Weistock M. Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 1986;37:681-687.
76. Wakshlak A, Weinstock M. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 1990;48:289-292.
77. Valee M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 1997;17: 2626-2636.
78. Koehl M, Le Maire V, Mayo W, Abrous DN, Maccari S, Piazza PV, Le Moal M, Valee M. Individual vulnerability of substance abuse and affective disorders: role of early environmental influences. Neurotoxicity Res 2002;4:281-296.
79. Piazza PV, Le Moal ML. Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids and dopaminergic neurons. Annu Rev Pharmacol Toxicol 1996;36:359-378.
80. Schneider ML, Coe CL, Lubach GR. Endocrine activation mimics the adverse effects of prenatal stress on the neuromotor development of the infant primate. Dev Psychobiol 1992;25:427-439.
81. Glover V. Maternal stress or anxiety in pregnancy and emotional development of the child. Br J Psychiatry 1997; 171:105-106.
82. Graham YP, Heim C, Goodman SH, et al. The effects of neonatal stress on brain development: implications for psychopathology. Dev Psychopathol 1999;11:545-565.
83. Weinstock M. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis. Neurosci Biobehav Rev 1997;21:1-10.
84. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the off-spring. Prog Neurobiol 2001;65:427-451.
85. Cladji C, Dioro J, Meaney MJ. Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 2000;48:1164-1174.
86. Francis DD, Diorio J, Plotsky PM, Meaney MJ. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 2002;22:7840-7843.
87. Levitt P, Reinoso B, Jones L. The critical impact of early cellular environment on neuronal development. Prev Med 1998;27:180-183.
88. Arbeille P, Maulik D, Salihagić-Kadić A, Locatelli A, Lansac J, Platt LD. Effect of long-term cocaine administration to pregnant ewes on fetal hemodynamics, oxygenation, and growth. Obstet Gynecol 1996;90:795-802.
89. Barker DJP. Fetal origins of coronary heart disease. BMJ 1995;311:171-174.
90. Carrera JM. Fetal ultrasonography: the first 40 years. Ultrasound Rev Obstet Gynecol 2004;4:141-147.
91. Hopkins B, Prechtl HFR. A qualitative approach to the development of movements during early infancy. In: Prechtl HFR, editor. Continuity of neural functions from perinatal to postnatal life. Oxford: Blackwell Scientific; 1984. pp 179-197.
92. Prechtl HFR. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev 1990;23:151-158.
93. Kainer F, Prechtl HF, Fngele H, Einspieler C. Assessment of the quality of general movements in fetuses and infants of women with type-I diabetes mellitus. Early Hum Dev 1997;50:13-25.
94. Sparling JW. Wilhelm IJ. Quantitative measurement of fetal movement: Fetal-Posture and Movement Assessment (F-PAM). Phys Occup Ther Pediatr 1993;12:97-114.
95. Kurjak A, Carrera JM, Stanojevic M, Andonotopo W, Azumendi G, Scazzocchio E, Medić M, Salihagić-Kadić A. The role of 4D sonography in the neurological assessment of early human development. Ultrasound Rev Obstet Gynecol 2004;4:148-159.
96. Kurjak A, Carrera JM, Medić M, Azumendi G, Andonotopo W, Stanojevic M. The antenatal development of fetal behavioral patterns assessed by four-dimensional sonography. J Matern Fetal Neonatal Med 2005; in press.
97. Kurjak A, Stanojevic M, Azumendi G, Carrera JM. The potential of four-dimensional (4D) ultrasonography in the assessment of fetal awareness. J Perinat Med 2005; 33:46-53.
98. Kurjak A, Stanojevic M, Andonotopo W, Scazzochio-Duenas E, Azumendi G, Carrera JM. Fetal behavior assessed in all three trimesters of normal pregnancy by four dimensional (4D) sonography. Croat Med J 2005; in press.
99. The Royal College of Obstetricians and Gynaecologists. Fetal awareness: report of a working party. London: RCOG Press; 1997.
100. Kurjak A. The beginning of human life and its modern scientific assessment. Clin Perinatol 2003;30:27-44.
101. Prechtl FHR. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev 1990;23:151-158.
102. Prechtl HFR. State of the art of a new functional assessment of the young nervous system. An early predictor of cerebral palsy. Early Hum Dev 1997;50:1-11.
103. Azumendi G, Kurjak A. Three-dimensional and four-dimensional sonography in the study of the fetal face. Ultrasound Rev Obstet Gynecol 2003;3:1-10.
104. Stanojevic M, Perlman JM, Andonotopo W, Kurjak A. From fetal to neonatal behavioral status. Ultrasound Rev Obstet Gynecol 2004;4:59-71.