In utero repair of myelomeningocele: Rationale, initial clinical experience and a randomized controlled prospective clinical trial

Neuroembryology and Aging

Volumn 4, Issue 4, 2006, Pages 165-174

  Danzer, Enrico ^a,b   Flake, Alan W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Fetus; In utero repair; Management of Myelomeningocele Study (MOMS); Myelomeningocele; Prenatal diagnosis

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; UTERUS SPASMOLYTIC AGENT;

AMNION FLUID; ARNOLD CHIARI MALFORMATION; BRAIN FUNCTION; BRAIN HERNIA; BRAIN VENTRICLE PERITONEUM SHUNT; CHEMICAL INJURY; CHRONIC DISEASE; CLINICAL FEATURE; CLINICAL STUDY; CLINICAL TRIAL; CONGENITAL MALFORMATION; CONTROLLED CLINICAL TRIAL; DISEASE COURSE; DISEASE SEVERITY; FETUS SURGERY; GESTATION PERIOD; HUMAN; INTERVENTION STUDY; MENINGOMYELOCELE; MULTIFACTORIAL GENETIC DISORDER; NEURULATION; NEWBORN MORTALITY; PERINATAL PERIOD; POSTNATAL CARE; PRENATAL DIAGNOSIS; PRIORITY JOURNAL; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; REVIEW; RHOMBENCEPHALON;

ANIMALIA;

EID: 41149092250     PISSN: 16613406     EISSN: 16613414     Source Type: Journal    
DOI: 10.1159/000118926     Document Type: Review

References (78)

1. Danzer E, Rintoul NE, Crombleholme TM, Adzick NS: Pathophysiology of neural tube defects;in Pollin R, Fox WW, Abman SH (eds): Fetal and Neonatal Physiology, ed 3. Philadelphia, Saunders, 2003, pp 1772-1785.
2. Dias MS, McLone DG: Hydrocephalus in the child with dysraphism. Neurosurg Clin N Am 1993;4:715-726.
3. Caldarelli M, DiRocco C, LaMarca F: Shunt complications in the first postoperative year in children with myelomeningocele. Childs Nerv Syst 1996;12:748-754.
4. Bell JE, Gordon A, Maloney AF: The association of hydrocephalus and Arnold-Chiari malformation with spina bifida in the fetus. Neuropathol Appl Neurobiol 1980;6:29-39.
5. Gilbert JN, Jones KL, Rorke LB, Chernoff GF, James HE: Central nervous system anomalies associated with myelomeningocele, hydrocephalus, and the Arnold-Chiari malformation: reappraisal of theories regarding the pathogenesis of posterior neural tube closure defects. Neurosurgery 1986;18:559-564.
6. Cochrane DD, Adderley R, White CP, Norman M, Steinbok P: Apnea in patients with myelomeningocele. Pediatr Neurosurg 1990;16:232-239.
7. Oaks W, Gaskill S: Symptomatic Chiari malformations in childhood;in Park T (ed): Spinal Dysraphism. Boston, Blackwell Scientific Publications, 1992, pp 104-125.
8. McLone DG, Knepper PA: The cause of Chiari II malformation: a unified theory. Pediatr Neurosci 1989;15:1-12.
9. Mitchell LE, Adzick NS, Melchionne J, Pasquariello PS, Sutton LN, Whitehead AS: Spina bifida. Lancet 2004;364:1885-1895.
10. Botto LD, Moore CA, Khoury MJ, Erickson JD: Neural-tube defects. N Engl J Med 1999;341:1509-1519.
11. Manning SM, Jennings R, Madsen JR: Pathophysiology, prevention, and potential treatment of neural tube defects. Ment Retard Dev Disabil Res Rev 2000;6:6-14.
12. Scott JM, Weir DG, Molloy A, McPartlin J, Daly L, Kirke P: Folic acid metabolism and mechanisms of neural tube defects. Ciba Found Symp 1994;181:180-187.
13. Czeizel AE, Dudas I: Prevention of the first occurrence of neural-tube defects by periconceptional vitamin supplementation. N Engl J Med 1992;327:1832-1835.
14. MRC Vitamin Study Research Group: Prevention of neural tube defects: results of the medical research council vitamin study. Lancet 1991;338:131-137.
15. Copp AJ, Bernfield M: Etiology and pathogenesis of human neural tube defects: insights from mouse models. Curr Opin Pediatr 1994;6:624-631.
16. Copp AJ, Greene ND, Murdoch JN: The genetic basis of mammalian neurulation. Nat Rev Genet 2003;4:784-793.
17. Copp AJ: Prevention of neural tube defects: vitamins, enzymes, and genes. Curr Opin Neurol 1998;11:97-102.
18. Harris MJ, Juriloff DM: Genetic landmarks for defects in mouse neural tube closure. Teratology 1997;56:177-187.
19. Melvin EC, George TM, Worley G, Franklin A, Mackey J, Viles K, Shah N, Drake CR, Enterline DS, Mclone D, Nye J, Oakes WJ, Mclaughlin C, Walker ML, Peterson P, Brei T, Buran C, Aben J, Ohm B, Bermans I, Qumsiyeh M, Vance, J, Pericak-Vance MA, Speer MC: Genetic studies in neural tube defects. NTD Collaborative Group. Pediatr Neurosurg 2000;32:1-9.
20. Edmonds LD, James LM: Temporal trends in the prevalence of congenital malformations at birth based on the birth defects monitoring program, United States, 1979-1987. MMWR Morb Mortal Wkly Rep 1990;39:19-23.
21. Lary JM, Edmonds LD: Prevalence of spina bifida at birth - United States, 1983-1990: a comparison to two surveillance systems. MMWR Morb Mortal Wkly Rep 1996;45:15-26.
22. Roberts HE, Moore CA, Cragan JD, Fernhoff PM, Khoury MJ: Impact of prenatal diagnosis on the birth prevalence of neural tube defects, Atlanta 1990-1991. Pediatrics 1995;96:880-883.
23. Velie EM, Shaw GM: Impact of prenatal diagnosis and elective termination on prevalence and risk estimates of neural tube defects in California, 1989-1991. Am J Epidemiol 1996;144:473-479.
24. Worly G, Schuster JM, Oakes WJ: Survival at 5 years of a cohort of newborn infants with myelomeningocele. Dev Med Child Neurol 1996;38:816-822.
25. Goodman RA: Economic burden of spina bifida - United States, 1980-1990. MMWR Morb Mortal Wkly Rep 1989;38:264-267.
26. Drugan A, Weissman A, Evans MI: Screening for neural tube defects. Clin Perinatol 2001;28:279-281.
27. Brock DJ, Sutcliffe RG: Alpha-fetoprotein in antenatal diagnosis of anencephaly and spina bifida. Lancet 1972;ii:197-199.
28. Loft AG: Determination of amniotic fluid acetylcholinesterase activity in the antenatal diagnosis of foetal malformations: the first ten years. J Clin Chem Clin Biochem 1990;28:893-911.
29. Simon EM, Pollock AN: Prenatal and postnatal imaging of spinal dysraphism. Semin Roentgenol 2004;39:182-196.
30. Patten B: Embryological stages in the establishing of myeloschisis with spina bifida. Am J Anat 1953;93:365-395.
31. Osaka K, Tanimura T, Hirayama A, Matsumoto S: Myelomeningocele before birth. J Neurosurg 1978;49:711-724.
32. Hutchins GM, Meuli M, Meuli-Simmen C, Jordan MA, Heffez DS, Blakemore KJ: Acquired spinal cord injury in human fetuses with myelomeningocele. Pediatr Pathol Lab Med 1996;16:701-712.
33. Meuli M, Meuli-Simmen C, Hutchins GM, Seller MJ, Harrison MR, Adzick NS: The spinal cord lesion in human fetuses with myelomeningocele: implications for fetal surgery. J Pediatr Surg 1997;31:448-452.
34. Korenromp MJ, Van Good JD, Bruinese HW, Kriek R: Early fetal movements in myelomeningocele. Lancet 1986;i:917-918.
35. Sival DA, Begeer JH, Staal-Schreinemachers AL, Vos-Niel JM, Beekhuis JR, Prechtl HF: Perinatal motor behavior and neurological outcome in spina bifida aperta. Early Hum Dev 1997;50:27-37.
36. Sival DA, Brouwer OF, Bruggink JL, Vies JS, Staal-Schreinemachers AL, Sollie KM, Sauer PJ, Bos AF: Movement analysis in neonates with spina bifida aperta. Early Hum Dev 2006;82:227-234.
37. Shurtleff DB, Luthy DA, Nyberg DA, Benedetti TJ, Mack LA: Meningomyelocele: management in utero and post partum. Ciba Found Symp 1994;181:270-280.
38. Luthy DA, Wardinsky T, Shurtleff DB, Hollenbach KA, Hickok DE, Nyberg DA, Benedetti TJ: Cesarean section before the onset of labor and subsequent motor function in infants with myelomeningocele diagnosed antenatally. N Engl J Med 1991;324:662-666.
39. Merrill DC, Goodwin P, Burson JM, Sato Y, Williamson R, Weiner CP: The optimal route of delivery for fetal myelomeningocele. Am J Obstet Gynecol 1998;179:235-240.
40. Cochrane D, Aronyk K, Sawatzky B, Wilson D, Steinbok P: The effects of labor and delivery on spinal cord function and ambulation in patients with myelomeningocele. Child Nerv Syst 1991;7:312-315.
41. Fleming A, Copp AJ: Embryonic folate metabolism and mouse neural tube defects. Science 1998;280:2107-2109.
42. Copp AJ, Brook FA, Roberts HJ: A cell-type-specific abnormality of cell proliferation in mutant (curly tail) mouse embryos developing spinal neural tube defects. Development 1988;104:285-295.
43. Van Straaten HW, Copp AJ: Curly tail: a 50-year history of the mouse spina bifida model. Anat Embryol 2001;203:225-237.
44. Selcuki M, Manning S, Bernfield M: The curly tail mouse model of human neural tube defects demonstrates normal spinal cord differentiation at the level of the meningomyelocele: implications for fetal surgery. Childs Nerv Syst 2001;17:19-23.
45. Duru S, Ceylan S, Ceylan S: Comparative effects of valproic acid sodium for Chiari-like malformation at 9 and 10 days of gestation in the rat. Childs Nerv Syst 2001;17:399-404.
46. Ehlers K, Elmazar MA, Nau H: Methionine reduces the valproic acid-induced spina bifida rate in mice without altering valproic acid kinetics. J Nutr 1996;126:67-75.
47. Ehlers K, Struje H, Merker HJ, Nau H: Spina bifida aperta induced by valproic acid and by all-trans-retinoic acid in the mouse: distinct differences in morphology and periods of sensitivity. Teratology 1992;46:117-130.
48. Michejda M: Intrauterine treatment of spina bifida. Primate model. Z Kinderchir 1984;39:259-261.
49. Heffez DS, Aryanpur J, Rotellini NA, Hutchins GM, Freeman JM: Intrauterine repair of experimental surgically created dysraphism. Neurosurgery 1993;32:1005-1010.
50. Heffez DS, Aryanpur J, Hutchins GM, Freeman JM: The paralysis associated with myelomeningocele: clinical and experimental data implicating a preventable spinal cord injury. Neurosurgery 1990;26:987-992.
51. Meuli M, Meuli-Simmen C, Yingling CD, Hoffman KB, Harrison MR, Adzick NS: A new model of myelomeningocele: studies in the fetal lamb. Surg Forum 1994;45:587-589.
52. Meuli M, Meuli-Simmen C, Hutchins GM, Yingling CD, Hoffman KM, Harrison MR, Adzick NS: In utero surgery rescues neurologic function at birth in sheep with spina bifida. Nat Med 1995;1:342-347.
53. Meuli M, Meuli-Simmen C, Hutchins GM, Yingling CD, Hutchins GM, Timmel GB, Harrison MR, Adzick NS: In utero repair of experimental myelomeningocele spares neurologic function at birth. J Pediatr Surg 1996;31:397-402.
54. Paek BW, Farmer DL, Wilkinson CC, Albanese CT, Peacook W, Harrison MR, Jennings RW: Hindbrain herniation develops in surgically created myelomeningocele but is absent after repair in fetal lambs. Am J Obstet Gynecol 2000;183:1119-1123.
55. Bouchard S, Davey MG, Rintoul NE, Walsh DS, Rorke LB, Adzick NS: Correction of hindbrain herniation and anatomy of the vermis following in utero repair of myelomeningocele in sheep. J Pediatr Surg 2003;38:451-458.
56. Danzer E, Schwarz U, Wehrli S, Radu A, Adzick NS, Flake AW: Retinoic acid induced myelomeningocele in fetal rats: characterization by histopathological analysis and magnetic resonance imaging. Exp Neurol 2005;194:467-475.
57. Danzer E, Kiddoo DA, Redden RA, Robinson L, Radu A, Zderic SA, Doolin EJ, Adzick NS, Flake AW: Structural and functional characterization of bladder smooth muscle in fetal rats with retinoic acid induced myelomeningocele. Am J Physiol Renal Physiol 2007;292:197-206.
58. Danzer E, Radu A, Volpe MA, Adzick NS, Flake AW: Normal neuromuscular development of the lower gastrointestinal tract and anorectum in fetal rats with retinoic acid induced myelomeningocele - implications for fetal surgery. J Am Coll Surg 2006;203:S36.
59. Adzick NS, Harrison MR: Fetal surgical therapy. Lancet 1994;343:897-902.
60. Danzer E, Sydorak RM, Harrison MR, Albanese CT: Minimal access fetal surgery. Eur J Obstet Gynecol Reprod Biol 2003;108:3-13.
61. Bruner J, Tulipan N, Richards W: Endoscopic coverage of fetal open myelomeningocele in utero. Am J Obstet Gynecol 1997;176:256-257.
62. Tulipan N, Bruner JP: Myelomeningocele repair in utero: a report of three cases. Pediatr Neurosurg 1998;28:177-180.
63. Adzick NS, Sutton LN, Crombleholme TM, Flake AW: Successful fetal surgery for spina bifida. Lancet 1998;352:1675-1676.
64. Johnson MP, Sutton LN Rintoul N, Crombleholme TM, Flake AW, Howell LJ, Hedrick HL, Wilson RD, Adzick NS: Fetal myelomeningocele repair: short-term clinical outcomes. Am J Obstet Gynecol 2003;189:482-487.
65. Sutton LN, Adzick NS, Bilaniuk LT, Johnson MP, Crombleholme TM, Flake AW: Improvement in hindbrain herniation demonstrated by serial fetal magnetic resonance imaging following fetal surgery for myelomeningocele. JAMA 1999;282:1826-1831.
66. Bruner JP, Tulipan N, Paschall RL, Boehm FH, Walsh WF, Silvia SR, Hernanz-Schulman M, Lowe LH, Reed GW: Fetal surgery for myelomeningocele and the incidence of shunt-dependent hydrocephalus. JAMA 1999;282:1819-1825.
67. Tulipan N, Sutton LN, Bruner JP, Cohen BM, Johnson M, Adzick NS: The effect of intrauterine myelomeningocele repair on the incidence of shunt-dependent hydrocephalus. Pediatr Neurosurg 2003;38:27-33.
68. Rintoul NE, Sutton LN, Hubbard AM, Cohen B, Melchionni J, Pasquariello PS, Adzick NS: A new look at myelomeningoceles: functional level, vertebral level, shunting, and the implications for fetal intervention. Pediatrics 2002;109:409-413.
69. Danzer E, Johnson MP, Wilson RD, Flake AW, Hedrick HL, Sutton LN, Adzick NS: fetal head biometry following in-utero repair of myelomeningocele. Ultrasound Obstet Gynecol 2004;24:606-611.
70. Danzer E, Johnson MP, Bebbington M, Simon EM, Wilson RD, Bilaniuk LT, Sutton LN, Adzick NS: Fetal head biometry assessed by fetal magnetic resonance imaging following in utero myelomeningocele repair. Fetal Diagn Ther 2007;22:1-6.
71. Johnson MP, Gerdes M, Rintoul N, Pasquariello P, Melchionni J, Sutton LN, Adzick NS: Maternal-fetal surgery for myelomeningocele: neurodevelopmental outcomes at 2 years of age. Am J Obstet Gynecol 2006;194:1145-1150.
72. Kollias SS, Goldstein RB, Cogen PH, Filly RA: Prenatally detected myelomeningoceles: sonographic accuracy in estimation of the spinal levels. Radiology 1992;185:109-112.
73. Biggio JR, Owen J, Wenstrom KD, Oakes WJ: Can prenatal ultrasound findings predict ambulatory status in fetuses with open spina bifida? Am J Obstet Gynecol 2001;185:1016-1020.
74. Tubbs S, Chambers MR, Smyth MD, Bartolucci AA, Bruner JP, Tulipan N, Oakes WJ: Late gestational intrauterine myelomeningocele repair does not improve lower extremity function. Pediatr Neurosurg 2003;38:128-132.
75. Danzer E, Adzick NS, Gerdes M, Bebbington MW, Sutton LN, Melchionni J, Johnson MP: Lower extremity neuromotor function following in utero myelomeningocele repair. Am J Obstet Gynecol 2006;195:S22.
76. Mazzola C, Albright AL, Sutton LN, Tuite GF, Hamilton RL, Pollack IF: Dermoid inclusion cysts and early spinal cord tethering after fetal surgery for myelomeningocele. N Engl J Med 2002;347:256-259.
77. Simpson JL: Fetal surgery for myelomeningocele: promise, progress, and problems. JAMA 1999;282:1873-1874.
78. Wilson RD, Johnson MP, Flake AW, Crombleholme TM, Hedrick HL, Wilson J, Adzick NS: Reproductive outcomes after pregnancy complicated by maternal-fetal surgery. Am J Obstet Gynecol 2004;191:1430-1436.