1932

Abstract

The International Fetal Medicine and Surgery Society was created in 1982 and proposed guidelines for fetal interventions that required demonstrations of the safety and feasibility of intended interventions in animal models prior to application in humans. Because of their short gestation and low cost, small animal models are useful in early investigation of fetal strategies. However, owing to the anatomic and physiologic differences between small animals and humans, repeated studies in large animal models are usually needed to facilitate translation to humans. Ovine (sheep) models have been used the most extensively to study the pathophysiology of congenital abnormalities and to develop techniques for fetal interventions. However, nonhuman primates have uterine and placental structures that most closely resemble those of humans. Thus, the nonhuman primate is the ideal model to develop surgical and anesthetic techniques that minimize obstetrical complications.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-030117-014637
2018-02-15
2024-10-11
Loading full text...

Full text loading...

/deliver/fulltext/animal/6/1/annurev-animal-030117-014637.html?itemId=/content/journals/10.1146/annurev-animal-030117-014637&mimeType=html&fmt=ahah

Literature Cited

  1. Liley AW. 1.  1963. Intrauterine transfusion of foetus in haemolytic disease. Br. Med. J. 21107–9
  2. Donald I, Macvicar J, Brown T. 2.  1958. Investigation of abdominal masses by pulsed ultrasound. Lancet 271:1188–95 [Google Scholar]
  3. Gottesfeld K, Thompson H, Holmes J, Taylor E. 3.  1967. Ultrasonic placentography: a new method for placental localization. Obstet. Gynecol. Surv. 22:250–52 [Google Scholar]
  4. Campbell S, Kohorn EI. 4.  1968. Placental localization by ultrasonic compound scanning. Int. J. Obstet. Gynaecol. 75:1007–13 [Google Scholar]
  5. Hobbins JC, Grannum PA, Berkowitz RL, Silverman R, Mahoney MJ. 5.  1979. Ultrasound in the diagnosis of congenital anomalies. Am. J. Obstet. Gynecol. 134:331–45 [Google Scholar]
  6. Garrett WJ, Kossoff G. 6.  1976. Selection of patients by ultrasonic echography for fetal and immediate neonatal surgery. J. Paediatr. Child Health 12:313–18 [Google Scholar]
  7. Harrison MR, Filly RA, Golbus MS, Berkowitz RL, Callen PW. 7.  et al. 1982. Fetal treatment; 1982. N. Engl. J. Med. 307:1651–52 [Google Scholar]
  8. Deprest JA, Devlieger R, Srisupundit K, Beck V, Sandaite I. 8.  et al. 2010. Fetal surgery is a clinical reality. Semin. Fetal Neonatal Med. 15:58–67 [Google Scholar]
  9. Sudhakaran N, Sothinathan U, Patel S. 9.  2012. Best practice guidelines: fetal surgery. Early Hum. Dev. 88:15–19 [Google Scholar]
  10. Iqbal CW, Hirose S, Lee H. 10.  2014. Fetal therapy. Ashcraft's Pediatric Surgery GW Holcomb III, JD Murphy, DJ Ostlie 132–44 London: Elsevier Health Sci. [Google Scholar]
  11. Østergaard G, Hansen HN, Ottesen JL. 11.  2010. Physiological, hematological, and clinical chemistry parameters (including conversion factors). Handbook of Laboratory Animal Science, Vol. I: Essential Principles and Practices 667–707 Boca Raton, FL: CRC, 3rd ed..
  12. Milani-Nejad N, Janssen PML. 12.  2014. Small and large animal models in cardiac contraction research: advantages and disadvantages. Pharmacol. Ther. 141:235–49 [Google Scholar]
  13. Hallock GG. 13.  1985. In utero cleft lip repair in A/J mice. Plast. Reconstr. Surg. 75:785–88 [Google Scholar]
  14. Schmidt AF, Goncalves FL, Figueira RL, Scorletti F, Peiro JL, Sbragia L. 14.  2016. Combined antenatal therapy with retinoic acid and tracheal occlusion in a rat model of congenital diaphragmatic hernia. Pediatr. Surg. Int. 32:591–98 [Google Scholar]
  15. Chun YS, Jung SJ. 15.  2007. The effect analysis and comparison between gastroschisis and tracheal ligation on experimental diaphragmatic hernia in fetal rabbits. J. Pediatr. Surg. 42:2030–34 [Google Scholar]
  16. Dionigi B, Ahmed A, Brazzo J III, Connors JP, Zurakowski D, Fauza DO. 16.  2015. Partial or complete coverage of experimental spina bifida by simple intra-amniotic injection of concentrated amniotic mesenchymal stem cells. J. Pediatr. Surg. 50:69–73 [Google Scholar]
  17. Pedreira DA, Valente PR, Abou-Jamra RC, Pelarigo CL, Silva LM, Goldenberg S. 17.  2003. Successful fetal surgery for the repair of a “myelomeningocele-like” defect created in the fetal rabbit. Fetal Diagn. Ther. 18:201–6 [Google Scholar]
  18. Goncalves FL, Bueno MP, Schmidt AF, Figueira RL, Sbragia L. 18.  2015. Treatment of bowel in experimental gastroschisis with a nitric oxide donor. Am. J. Obstet. Gynecol. 212:383.e1–7 [Google Scholar]
  19. Aoki Y, Ohshio T, Komi N. 19.  1980. An experimental study on gastroschisis using fetal surgery. J. Pediatr. Surg. 15:252–56 [Google Scholar]
  20. Lopez-Fernandez S, Encinas JL, Hernández-Martín S, Vilanova A, Sánchez A. 20.  et al. 2013. Experimental model of amniotic band in rats: model description and initial morphological study. Cir. Pediatr. 26:177–82 [Google Scholar]
  21. Saiki Y, Konig A, Waddell J, Rebeyka IM. 21.  1997. Hemodynamic alteration by fetal surgery accelerates myocyte proliferation in fetal guinea pig hearts. Surgery 122:412–19 [Google Scholar]
  22. Tibboel D, Molenaar JC, Van Nie CJ. 22.  1979. New perspectives in fetal surgery: the chicken embryo. J. Pediatr. Surg. 14:438–40 [Google Scholar]
  23. Moran CJ, Ramesh A, Brama PAJ, O'Byrne JM, O'Brien FJ, Levingstone TJ. 23.  2016. The benefits and limitations of animal models for translational research in cartilage repair. J. Exp. Orthop. 3:1 [Google Scholar]
  24. Weinzweig J, Panter KE, Spangenberger A, Harper JS, McRae R, Edstrom LE. 24.  2002. The fetal cleft palate: III. Ultrastructural and functional analysis of palatal development following in utero repair of the congenital model. Plast. Reconstr. Surg. 109:2355–62 [Google Scholar]
  25. Kuroda T, Saeki M, Tanaka K, Komura M, Honna T. 25.  et al. 1998. The combined method: a novel access technique for fetal endoscopic surgery. J. Pediatr. Surg. 33:1641–44 [Google Scholar]
  26. Barnard C. 26.  1957. A method of operating on fetal dogs in utero. Surgery 41:805–7 [Google Scholar]
  27. Swindle MM, Wiest DB, Smith AC, Garner SS, Case CC. 27.  et al. 1996. Fetal surgical protocols in Yucatan miniature swine. Lab. Anim. Sci. 46:90–95 [Google Scholar]
  28. Harrison MR, Anderson J, Rosen MA, Ross NA, Hendrickx AG. 28.  1982. Fetal surgery in the primate I. Anesthetic, surgical, and tocolytic management to maximize fetal-neonatal survival. J. Pediatr. Surg. 17:115–22 [Google Scholar]
  29. Harrison MR, Bressack MA, Churg AM, de Lorimier AA. 29.  1980. Correction of congenital diaphragmatic hernia in utero. II. Simulated correction permits fetal lung growth with survival at birth. Surgery 88:260–68 [Google Scholar]
  30. Harrison MR, Ross N, Noall R, de Lorimier AA. 30.  1983. Correction of congenital hydronephrosis in utero. I. The model: Fetal urethral obstruction produces hydronephrosis and pulmonary hypoplasia in fetal lambs. J. Pediatr. Surg. 18:247–56 [Google Scholar]
  31. Wang A, Brown EG, Lankford L, Keller BA, Pivetti CD. 31.  et al. 2015. Placental mesenchymal stromal cells rescue ambulation in ovine myelomeningocele. Stem Cells Transl. Med. 4:659–69 [Google Scholar]
  32. Langer JC, Bell JG, Castillo RO, Crombleholme TM, Longaker MT. 32.  et al. 1990. Etiology of intestinal damage in gastroschisis, II. Timing and reversibility of histological changes, mucosal function, and contractility. J. Pediatr. Surg. 25:1122–26 [Google Scholar]
  33. Turley K, Vlahakes GJ, Harrison MR, Messina L, Hanley F. 33.  et al. 1982. Intrauterine cardiothoracic surgery: the fetal lamb model. Ann. Thorac. Surg. 34:422–26 [Google Scholar]
  34. Crombleholme TM, Dirkes K, Whitney TM, Alman B, Garmel S, Connelly RJ. 34.  1995. Amniotic band syndrome in fetal lambs. I: fetoscopic release and morphometric outcome. J. Pediatr. Surg. 30:974–78 [Google Scholar]
  35. Evans ML, Oberg KC, Kirsch W, Zhu YH, Hardesty RA. 35.  1995. Intrauterine repair of cleft lip-like defects in lambs with a novel microclip. J. Craniofac. Surg. 6:126–31 [Google Scholar]
  36. Ngamprasertwong P, Michelfelder EC, Arbabi S, Choi YS, Statile C. 36.  et al. 2013. Anesthetic techniques for fetal surgery: effects of maternal anesthesia on intraoperative fetal outcomes in a sheep model. Anesthesiology 118:796–808 [Google Scholar]
  37. Kohl T, Ziemann M, Weinbach J, Tchatcheva K, Gembruch U, Hasselblatt M. 37.  2010. Partial amniotic carbon dioxide insufflation during minimally invasive fetoscopic interventions seems safe for the fetal brain in sheep. J. Laparoendosc. Adv. Surg. Tech. A 20:651–53 [Google Scholar]
  38. Knight CG, Lorincz A, Johnson A, Gidell K, Rabah R. 38.  et al. 2004. Robot-enhanced fetoscopic surgery. J. Pediatr. Surg. 39:1463–65 [Google Scholar]
  39. Nakayama DK, Harrison MR, Seron-Ferre M, Villa RL. 39.  1984. Fetal surgery in the primate II. Uterine electromyographic response to operative procedures and pharmacologic agents. J. Pediatr. Surg. 19:333–39 [Google Scholar]
  40. Adzick NS, Harrison MR, Glick PL, Anderson J, Villa RL. 40.  et al. 1986. Fetal surgery in the primate III. Maternal outcome after fetal surgery. J. Pediatr. Surg. 21:477–80 [Google Scholar]
  41. Sananes N, Ruano R, Weingertner AS, Regnard P, Salmon Y. 41.  et al. 2015. Experimental fetal endoscopic tracheal occlusion in rhesus and cynomolgus monkeys: nonhuman primate models. J. Matern. Fetal Neonatal Med. 28:1822–27 [Google Scholar]
  42. Michejda M. 42.  1984. Intrauterine treatment of spina bifida: primate model. Eur. J. Pediatr. Surg. 39:259–61 [Google Scholar]
  43. Wooding P, Burton G. 43.  2008. Comparative Placentation: Structures, Functions and Evolution Dordrecht, Neth: Springer Sci. Bus. Media [Google Scholar]
  44. Ramsey EM. 44.  1982. The Placenta: Human and Animal Santa Barbara, CA: Praeger [Google Scholar]
  45. VandeBerg JL, Williams‐Blangero S. 45.  1997. Advantages and limitations of nonhuman primates as animal models in genetic research on complex diseases. J. Med. Primatol. 26:113–19 [Google Scholar]
  46. Oberg KC, Robles AE, Ducsay CA, Rasi CR, Rouse GA. 46.  et al. 1999. Endoscopic intrauterine surgery in primates: overcoming technical obstacles. Surg. Endosc. 13:420–26 [Google Scholar]
  47. Thomasson BH, Ravitch MM. 47.  1969. Fetal surgery in the rabbit. Surgery 66:1092–102 [Google Scholar]
  48. Nelson JM, Krummel TM, Haynes JH, Flood LC, Sauer L. 48.  et al. 1990. Operative techniques in the fetal rabbit. J. Investig. Surg. 3:393–98 [Google Scholar]
  49. Kilby MD, Johnson A, Oepkes D. 49.  2013. Fetal Therapy: Scientific Basis and Critical Appraisal of Clinical Benefits Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  50. Irish MS, Glick PL, Russell J, Kapur P, Bambini DA. 50.  et al. 1998. Contractile properties of intralobar pulmonary arteries and veins in the fetal lamb model of congenital diaphragmatic hernia. J. Pediatr. Surg. 33:921–28 [Google Scholar]
  51. Glick PL, Stannard VA, Leach CL, Rossman J, Hosada Y. 51.  et al. 1992. Pathophysiology of congenital diaphragmatic hernia. II: The fetal lamb CDH model is surfactant deficient. J. Pediatr. Surg. 27:382–88 [Google Scholar]
  52. Harrison MR, Langer JC, Adzick NS, Golbus MS, Filly RA. 52.  et al. 1990. Correction of congenital diaphragmatic hernia in utero, V. Initial clinical experience. J. Pediatr. Surg. 25:47–57 [Google Scholar]
  53. Harrison MR, Adzick NS, Flake AW, Jennings RW, Estes JM. 53.  et al. 1993. Correction of congenital diaphragmatic hernia in utero: VI. Hard-earned lessons. J. Pediatr. Surg. 28:1411–18 [Google Scholar]
  54. Harrison MR, Adzick NS, Bullard KM, Farrell JA, Howell LJ. 54.  et al. 1997. Correction of congenital diaphragmatic hernia in utero VII: a prospective trial. J. Pediatr. Surg. 32:1637–42 [Google Scholar]
  55. Carmel JA, Friedman F, Adams FH. 55.  1965. Fetal tracheal ligation and lung development. Am. J. Dis. Child. 109:452–56 [Google Scholar]
  56. Beierle EA, Langham MR, Cassin S. 56.  1996. In utero lung growth of fetal sheep with diaphragmatic hernia and tracheal stenosis. J. Pediatr. Surg. 31:141–47 [Google Scholar]
  57. Luks FI, Gilchrist BF, Jackson BT, Piasecki GJ. 57.  1996. Endoscopic tracheal obstruction with an expanding device in a fetal lamb model: preliminary considerations. Fetal Diagn. Ther. 11:67–71 [Google Scholar]
  58. Harrison MR, Adzick NS, Flake AW, VanderWall KJ, Bealer JF. 58.  et al. 1996. Correction of congenital diaphragmatic hernia in utero VIII: response of the hypoplastic lung to tracheal occlusion. J. Pediatr. Surg. 31:1339–48 [Google Scholar]
  59. Harrison MR, Mychaliska GB, Albanese CT, Jennings RW, Farrell JA. 59.  et al. 1998. Correction of congenital diaphragmatic hernia in utero IX: Fetuses with poor prognosis (liver herniation and low lung-to-head ratio) can be saved by fetoscopic temporary tracheal occlusion. J. Pediatr. Surg. 33:1017–23 [Google Scholar]
  60. Harrison MR, Keller RL, Hawgood SB, Kitterman JA, Sandberg PL. 60.  et al. 2003. A randomized trial of fetal endoscopic tracheal occlusion for severe fetal congenital diaphragmatic hernia. N. Engl. J. Med. 349:1916–24 [Google Scholar]
  61. Saddiq WB, Piedboeuf B, Laberge J-M, Gamache M, Petrov P. 61.  et al. 1997. The effects of tracheal occlusion and release on type II pneumocytes in fetal lambs. J. Pediatr. Surg. 32:834–38 [Google Scholar]
  62. Cannie MM, Jani JC, Keyzer FD, Allegaert K, Dymarkowski S, Deprest J. 62.  2009. Evidence and patterns in lung response after fetal tracheal occlusion: clinical controlled study. Radiology 252:526–33 [Google Scholar]
  63. Jani JC, Nicolaides KH, Gratacós E, Valencia CM, Doné E. 63.  et al. 2009. Severe diaphragmatic hernia treated by fetal endoscopic tracheal occlusion. Ultrasound Obstet. Gynecol. 34:304–10 [Google Scholar]
  64. Crombleholme TM, Coleman B, Hedrick H, Liechty K, Howell L. 64.  et al. 2002. Cystic adenomatoid malformation volume ratio predicts outcome in prenatally diagnosed cystic adenomatoid malformation of the lung. J. Pediatr. Surg. 37:331–38 [Google Scholar]
  65. Adzick NS, Harrison MR, Crombleholme TM, Flake AW, Howell LJ. 65.  1998. Fetal lung lesions: management and outcome. Am. J. Obstet. Gynecol. 179:884–89 [Google Scholar]
  66. Andersen HM, Drew JH, Beischer NA, Hutchison AA, Fortune DW. 66.  1983. Non-immune hydrops fetalis: changing contribution to perinatal mortality. Int. J. Obstet. Gynaecol. 90:636–39 [Google Scholar]
  67. Rice HE, Estes JM, Hedrick MH, Bealer JF, Harrison MR, Adzick NS. 67.  1994. Congenital cystic adenomatoid malformation: a sheep model of fetal hydrops. J. Pediatr. Surg. 29:692–96 [Google Scholar]
  68. Evans M, Adzick N, Holzgreve W, Harrison M. 68.  2001. The Unborn Patient: The Art and Science of Fetal Therapy Philadelphia: W.B. Saunders Co. [Google Scholar]
  69. Cavoretto P, Molina F, Poggi S, Davenport M, Nicolaides KH. 69.  2008. Prenatal diagnosis and outcome of echogenic fetal lung lesions. Ultrasound Obstet. Gynecol. 32:769–83 [Google Scholar]
  70. Tsao K, Hawgood S, Vu L, Hirose S, Sydorak R. 70.  et al. 2003. Resolution of hydrops fetalis in congenital cystic adenomatoid malformation after prenatal steroid therapy. J. Pediatr. Surg. 38:508–10 [Google Scholar]
  71. Peranteau WH, Wilson RD, Liechty KW, Johnson MP, Bebbington MW. 71.  et al. 2007. Effect of maternal betamethasone administration on prenatal congenital cystic adenomatoid malformation growth and fetal survival. Fetal Diagn. Ther. 22:365–71 [Google Scholar]
  72. Curran PF, Jelin EB, Rand L, Hirose S, Feldstein VA. 72.  et al. 2010. Prenatal steroids for microcystic congenital cystic adenomatoid malformations. J. Pediatr. Surg. 45:145–50 [Google Scholar]
  73. Tchervenkov CI, Jacobs ML, Tahta SA. 73.  2000. Congenital heart surgery nomenclature and database project: hypoplastic left heart syndrome. Ann. Thorac. Surg. 69:170–79 [Google Scholar]
  74. Morris CD, Outcalt J, Menashe VD. 74.  1990. Hypoplastic left heart syndrome: natural history in a geographically defined population. Pediatrics 85:977–83 [Google Scholar]
  75. Norwood WI, Kirklin JK, Sanders SP. 75.  1980. Hypoplastic left heart syndrome: experience with palliative surgery. Am. J. Cardiol. 45:87–91 [Google Scholar]
  76. Tweddell JS, Hoffman GM, Mussatto KA, Fedderly RT, Berger S. 76.  et al. 2002. Improved survival of patients undergoing palliation of hypoplastic left heart syndrome: lessons learned from 115 consecutive patients. Circulation 106:I–82I-89 [Google Scholar]
  77. Tabbutt S, Dominguez TE, Ravishankar C, Marino BS, Gruber PJ. 77.  et al. 2005. Outcomes after the stage I reconstruction comparing the right ventricular to pulmonary artery conduit with the modified Blalock Taussig shunt. Ann. Thorac. Surg. 80:1582–91 [Google Scholar]
  78. d'Udekem Y, Xu MY, Galati JC, Lu S, Iyengar AJ. 78.  et al. 2012. Predictors of survival after single-ventricle palliation: the impact of right ventricular dominance. J. Am. Coll. Cardiol. 59:1178–85 [Google Scholar]
  79. Mahle WT, Spray TL, Wernovsky G, Gaynor JW, Clark BJ. 79.  2000. Survival after reconstructive surgery for hypoplastic left heart syndrome. Circulation 102:III–136III-41 [Google Scholar]
  80. Simpson JM, Sharland GK. 80.  1997. Natural history and outcome of aortic stenosis diagnosed prenatally. Heart 77:205–10 [Google Scholar]
  81. Bical O, Gallix P, Toussaint M, Hero M, Karam J. 81.  et al. 1987. Intrauterine creation and repair of pulmonary artery stenosis in the fetal lamb: weight and ultrastructural changes of the ventricles. J. Thorac. Cardiovasc. Surg. 93:761–66 [Google Scholar]
  82. Slate R, Stevens M, Verrier ED. 82.  1985. Intrauterine repair of pulmonary stenosis in fetal sheep. Surg. Forum 36:246–47 [Google Scholar]
  83. McElhinney DB, Marshall AC, Wilkins-Haug LE, Brown DW, Benson CB. 83.  et al. 2009. Predictors of technical success and postnatal biventricular outcome after in utero aortic valvuloplasty for aortic stenosis with evolving hypoplastic left heart syndrome. Circulation 120:1482–90 [Google Scholar]
  84. Vlahos AP, Lock JE, McElhinney DB, van der Velde ME. 84.  2004. Hypoplastic left heart syndrome with intact or highly restrictive atrial septum. Circulation 109:2326–30 [Google Scholar]
  85. Marshall AC, Levine J, Morash D, Silva V, Lock JE. 85.  et al. 2008. Results of in utero atrial septoplasty in fetuses with hypoplastic left heart syndrome. Prenat. Diagn. 28:1023–28 [Google Scholar]
  86. Tulzer G, Arzt W, Franklin RCG, Loughna PV, Mair R, Gardiner HM. 86.  2002. Fetal pulmonary valvuloplasty for critical pulmonary stenosis or atresia with intact septum. Lancet 360:1567–68 [Google Scholar]
  87. Kabagambe S, Chen Y, Farmer D. 87.  2016. Fetal surgery for myelomeningocele: current clinical practice and translational research. Minerva Pediatr 69:59–65 [Google Scholar]
  88. Adzick NS. 88.  2010. Fetal myelomeningocele: natural history, pathophysiology, and in-utero intervention. Semin. Fetal Neonatal Med. 15:9–14 [Google Scholar]
  89. Heffez DS, Aryanpur J, Hutchins GM, Freeman JM. 89.  1990. The paralysis associated with myelomeningocele: clinical and experimental data implicating a preventable spinal cord injury. Neurosurgery 26:987–92 [Google Scholar]
  90. Paek BW, Farmer DL, Wilkinson CC, Albanese CT, Peacock W. 90.  et al. 2000. Hindbrain herniation develops in surgically created myelomeningocele but is absent after repair in fetal lambs. Am. J. Obstet. Gynecol. 183:1119–23 [Google Scholar]
  91. von Koch CS, Compagnone N, Hirose S, Yoder S, Harrison MR, Farmer DL. 91.  2005. Myelomeningocele: characterization of a surgically induced sheep model and its central nervous system similarities and differences to the human disease. Am. J. Obstet. Gynecol. 193:1456–62 [Google Scholar]
  92. Julia V, Sancho MA, Albert A, Conill J, Martinez A. 92.  et al. 2006. Prenatal covering of the spinal cord decreases neurologic sequelae in a myelomeningocele model. J. Pediatr. Surg. 41:1125–29 [Google Scholar]
  93. Bouchard S, Davey MG, Rintoul NE, Walsh DS, Rorke LB, Adzick NS. 93.  2003. Correction of hindbrain herniation and anatomy of the vermis after in utero repair of myelomeningocele in sheep. J. Pediatr. Surg. 38:451–58; discussion 51–58 [Google Scholar]
  94. Adzick NS, Thom EA, Spong CY, Brock JW III, Burrows PK. 94.  et al. 2011. A randomized trial of prenatal versus postnatal repair of myelomeningocele. N. Engl. J. Med. 364:993–1004 [Google Scholar]
  95. Johnson MP, Bennett KA, Rand L, Burrows PK, Thom EA. 95.  et al. 2016. The Management of Myelomeningocele study: obstetrical outcomes and risk factors for obstetrical complications following prenatal surgery. Am. J. Obstet. Gynecol. 215:778.e1–e9 [Google Scholar]
  96. Pedreira DA, Zanon N, Nishikuni K, Moreira de Sá RA, Acacio GL. 96.  et al. 2016. Endoscopic surgery for the antenatal treatment of myelomeningocele: the CECAM trial. Am. J. Obstet. Gynecol. 214:111.e1–e11 [Google Scholar]
  97. Degenhardt J, Schurg R, Winarno A, Oehmke F, Khaleeva A. 97.  et al. 2014. Percutaneous minimal-access fetoscopic surgery for spina bifida aperta. Part II: maternal management and outcome. Ultrasound Obstet. Gynecol. 44:525–31 [Google Scholar]
  98. Joyeux L, Engels AC, Russo FM, Jimenez J, Van Mieghem T. 98.  et al. 2016. Fetoscopic versus open repair for spina bifida aperta: a systematic review of outcomes. Fetal Diagn. Ther. 39:161–71 [Google Scholar]
  99. Araujo Junior E, Eggink AJ, van den Dobbelsteen J, Martins WP, Oepkes D. 99.  2016. Procedure-related complications of open versus endoscopic fetal surgery for treatment of spina bifida in an era of intrauterine myelomeningocele repair: systematic review and meta-analysis. Ultrasound Obstet. Gynecol. 48:151–60 [Google Scholar]
  100. Kabagambe SK, Chen YJ, Vanover MA, Saadai P, Farmer DL. 100.  2017. New directions in fetal surgery for myelomeningocele. Child's Nerv. Syst. 33:1185–90 [Google Scholar]
  101. Belfort MA, Whitehead WE, Shamshirsaz AA, Bateni ZH, Olutoye OO. 101.  et al. 2017. Fetoscopic open neural tube defect repair: development and refinement of a two-port, carbon dioxide insufflation technique. Obstet. Gynecol. 129:734–43 [Google Scholar]
  102. Dionigi B, Brazzo JA III, Ahmed A, Feng C, Wu Y. 102.  et al. 2015. Trans-amniotic stem cell therapy (TRASCET) minimizes Chiari-II malformation in experimental spina bifida. J. Pediatr. Surg. 50:1037–41 [Google Scholar]
  103. Feng C, Graham CD, Connors JP, Brazzo J III, Zurakowski D, Fauza DO. 103.  2016. A comparison between placental and amniotic mesenchymal stem cells for transamniotic stem cell therapy (TRASCET) in experimental spina bifida. J. Pediatr. Surg. 51:1010–13 [Google Scholar]
  104. Watanabe M, Jo J-i, Radu A, Kaneko M, Tabata Y, Flake AW. 104.  2010. A tissue engineering approach for prenatal closure of myelomeningocele with gelatin sponges incorporating basic fibroblast growth factor. Tissue Eng. A 16:1645–55 [Google Scholar]
  105. Watanabe M, Li H, Roybal J, Santore M, Radu A. 105.  et al. 2011. A tissue engineering approach for prenatal closure of myelomeningocele: comparison of gelatin sponge and microsphere scaffolds and bioactive protein coatings. Tissue Eng. A 17:1099–110 [Google Scholar]
  106. Watanabe M, Li H, Kim AG, Weilerstein A, Radu A. 106.  et al. 2016. Complete tissue coverage achieved by scaffold-based tissue engineering in the fetal sheep model of myelomeningocele. Biomaterials 76:133–43 [Google Scholar]
  107. Brown EG, Keller BA, Lankford L, Pivetti CD, Hirose S. 107.  et al. 2016. Age does matter: a pilot comparison of placenta-derived stromal cells for in utero repair of myelomeningocele using a lamb model. Fetal Diagn. Ther. 39:179–85 [Google Scholar]
  108. Brown EG, Keller BA, Pivetti CD, Sitkin NA, Wang A. 108.  et al. 2015. Development of a locomotor rating scale for testing motor function in sheep. J. Pediatr. Surg. 50:617–21 [Google Scholar]
  109. Altman RP, Randolph JG, Lilly JR. 109.  1974. Sacrococcygeal teratoma: American Academy of Pediatrics surgical section survey-1973. J. Pediatr. Surg. 9:389–98 [Google Scholar]
  110. Adzick NS, Crombleholme TM, Morgan MA, Quinn TM. 110.  1997. A rapidly growing fetal teratoma. Lancet 349:538 [Google Scholar]
  111. Hedrick HL, Flake AW, Crombleholme TM, Howell LJ, Johnson MP. 111.  et al. 2004. Sacrococcygeal teratoma: prenatal assessment, fetal intervention, and outcome. J. Pediatr. Surg. 39:430–38 [Google Scholar]
  112. Flake AW, Harrison MR, Adzick NS, Laberge J-M, Warsof SL. 112.  1986. Fetal sacrococcygeal teratoma. J. Pediatr. Surg. 21:563–66 [Google Scholar]
  113. Langer JC, Harrison MR, Schmidt KG, Silverman NH, Anderson RL. 113.  et al. 1989. Fetal hydrops and death from sacrococcygeal teratoma: rationale for fetal surgery. Am. J. Obstet. Gynecol. 160:1145–50 [Google Scholar]
  114. Paek BW, Jennings RW, Harrison MR, Filly RA, Tacy TA. 114.  et al. 2001. Radiofrequency ablation of human fetal sacrococcygeal teratoma. Am. J. Obstet. Gynecol. 184:503–7 [Google Scholar]
  115. Ruano R, Duarte S, Zugaib M. 115.  2009. Percutaneous laser ablation of sacrococcygeal teratoma in a hydropic fetus with severe heart failure—too late for a surgical procedure?. Fetal Diagn. Ther. 25:26–30 [Google Scholar]
  116. Dinneen MD, Dhillon HK, Ward HC, Duffy PG, Ransley PG. 116.  1993. Antenatal diagnosis of posterior urethral valves. Br. J. Urol. 72:364–69 [Google Scholar]
  117. Malin G, Tonks AM, Morris RK, Gardosi J, Kilby MD. 117.  2012. Congenital lower urinary tract obstruction: a population-based epidemiological study. Int. J. Obstet. Gynaecol. 119:1455–64 [Google Scholar]
  118. Nakayama DK, Harrison MR, de Lorimier AA. 118.  1986. Prognosis of posterior urethral valves presenting at birth. J. Pediatr. Surg. 21:43–45 [Google Scholar]
  119. Mahony BS, Callen PW, Filly RA. 119.  1985. Fetal urethral obstruction: US evaluation. Radiology 157:221–24 [Google Scholar]
  120. Harrison MR, Nakayama DK, Noall R, de Lorimier AA. 120.  1982. Correction of congenital hydronephrosis in utero II. Decompression reverses the effects of obstruction on the fetal lung and urinary tract. J. Pediatr. Surg. 17:965–74 [Google Scholar]
  121. McVary KT, Maizels M. 121.  1989. Urinary obstruction reduces glomerulogenesis in the developing kidney: a model in the rabbit. J. Urol. 142:646–51; discussion 67–68 [Google Scholar]
  122. Crombleholme TM, Harrison MR, Langer JC, Longaker MT, Anderson RL. 122.  et al. 1988. Early experience with open fetal surgery for congenital hydronephrosis. J. Pediatr. Surg. 23:1114–21 [Google Scholar]
  123. Harrison MR, Golbus MS, Filly RA, Nakayama DK, Callen PW. 123.  et al. 1982. Management of the fetus with congenital hydronephrosis. J. Pediatr. Surg. 17:728–42 [Google Scholar]
  124. Quintero RA, Hume R, Smith C, Johnson MP, Cotton DB. 124.  et al. 1995. Percutaneous fetal cystoscopy and endoscopic fulguration of posterior urethral valves. Am. J. Obstet. Gynecol. 172:206–9 [Google Scholar]
  125. Ruano R, Duarte S, Bunduki V, Giron AM, Srougi M, Zugaib M. 125.  2010. Fetal cystoscopy for severe lower urinary tract obstruction—initial experience of a single center. Prenat. Diagn. 30:30–39 [Google Scholar]
  126. Sebire NJ, Snijders RJM, Hughes K, Sepulveda W, Nicolaides KH. 126.  1997. The hidden mortality of monochorionic twin pregnancies. Int. J. Obstet. Gynaecol. 104:1203–7 [Google Scholar]
  127. Simpson LL. 127.  2013. Twin-twin transfusion syndrome. Am. J. Obstet. Gynecol. 208:3–18 [Google Scholar]
  128. Fusi L, McParland P, Fisk N, Nicolini U, Wigglesworth J. 128.  1991. Acute twin-twin transfusion: a possible mechanism for brain-damaged survivors after intrauterine death of a monochorionic twin. Obstet. Gynecol. 78:517–20 [Google Scholar]
  129. Quintero RA, Dickinson JE, Morales WJ, Bornick PW, Bermúdez C. 129.  et al. 2003. Stage-based treatment of twin-twin transfusion syndrome. Am. J. Obstet. Gynecol. 188:1333–40 [Google Scholar]
  130. Saunders NJ, Snijders RJM, Nicolaides KH. 130.  1992. Therapeutic amniocentesis in twin-twin transfusion syndrome appearing in the second trimester of pregnancy. Am. J. Obstet. Gynecol. 166:820–24 [Google Scholar]
  131. Johnson JR, Rossi KQ, O'Shaughnessy RW. 131.  2001. Amnioreduction versus septostomy in twin-twin transfusion syndrome. Am. J. Obstet. Gynecol. 185:1044–47 [Google Scholar]
  132. Deprest JA, Audibert F, Van Schoubroeck D Hecher K, Mahieu-Caputo D. 132.  2000. Bipolar coagulation of the umbilical cord in complicated monochorionic twin pregnancy. Am. J. Obstet. Gynecol. 182:340–45 [Google Scholar]
  133. DeLia JE, Rogers JG, Dixon JA. 133.  1985. Treatment of placental vasculature with a neodymium-yttrium-aluminum-garnet laser via fetoscopy. Am. J. Obstet. Gynecol. 151:1126–27 [Google Scholar]
  134. Delia JE, Cukierski MA, Lundergan DK, Kochenour NK. 134.  1989. Neodymium: yttrium-aluminum-garnet laser occlusion of rhesus placental vasculature via fetoscopy. Am. J. Obstet. Gynecol. 160:485–89 [Google Scholar]
  135. Senat M-V, Deprest J, Boulvain M, Paupe A, Winer N, Ville Y. 135.  2004. Endoscopic laser surgery versus serial amnioreduction for severe twin-to-twin transfusion syndrome. N. Engl. J. Med. 351:136–44 [Google Scholar]
  136. Robie GF, Payne GG Jr, Morgan MA. 136.  1989. Selective delivery of an acardiac, acephalic twin. N. Engl. J. Med. 320:512–13 [Google Scholar]
  137. Tsao K, Feldstein VA, Albanese CT, Sandberg PL, Lee H. 137.  et al. 2002. Selective reduction of acardiac twin by radiofrequency ablation. Am. J. Obstet. Gynecol. 187:635–40 [Google Scholar]
  138. Lee H, Wagner AJ, Sy E, Ball R, Feldstein VA. 138.  et al. 2007. Efficacy of radiofrequency ablation for twin-reversed arterial perfusion sequence. Am. J. Obstet. Gynecol. 196:459.e1–e4 [Google Scholar]
  139. Rowsell AR. 139.  1989. The amniotic band disruption complex: the pathogenesis of oblique facial clefts; an experimental study in the foetal rat. Br. J. Plast. Surg. 42:291–95 [Google Scholar]
  140. Rowsell AR. 140.  1988. The amniotic band disruption complex: the pathogenesis of congenital limb ring-constrictions; an experimental study in the foetal rat. Br. J. Plast. Surg. 41:45–51 [Google Scholar]
  141. Keswani SG, Johnson MP, Adzick NS, Hori S, Howell LJ. 141.  et al. 2003. In utero limb salvage: fetoscopic release of amniotic bands for threatened limb amputation. J. Pediatr. Surg. 38:848–51 [Google Scholar]
  142. Peiró JL, Carreras E, Soldado F, Sanchez-Duran MA, Aguirre M. 142.  et al. 2009. Fetoscopic release of umbilical cord amniotic band in a human fetus. Ultrasound Obstet. Gynecol. 33:232–34 [Google Scholar]
  143. Hüsler MR, Wilson RD, Horii SC, Bebbington MW, Adzick NS, Johnson MP. 143.  2009. When is fetoscopic release of amniotic bands indicated? Review of outcome of cases treated in utero and selection criteria for fetal surgery. Prenat. Diagn. 29:457–63 [Google Scholar]
  144. Michejda M, Hodgen GD. 144.  1981. In utero diagnosis and treatment of non-human primate fetal skeletal anomalies: I. hydrocephalus. JAMA 246:1093–97 [Google Scholar]
  145. Glick PL, Harrison MR, Halks-Miller M, Adzick NS, Nakayama DK. 145.  et al. 1984. Correction of congenital hydrocephalus in utero II: efficacy of in utero shunting. J. Pediatr. Surg. 19:870–81 [Google Scholar]
  146. Manning FA, Harrison MR, Rodeck C. 146.  1986. Catheter shunts for fetal hydronephrosis and hydrocephalus. N. Engl. J. Med. 315:336–40 [Google Scholar]
  147. Cavalheiro S, Moron AF, Almodin CG, Suriano IC, Hisaba V. 147.  et al. 2011. Fetal hydrocephalus. Child's Nerv. Syst. 27:1575 [Google Scholar]
  148. Longaker MT, Dodson TB, Kaban LB. 148.  1990. A rabbit model for fetal cleft lip repair. J. Oral Maxillofac. Surg. 48:714–19 [Google Scholar]
  149. Weinzweig J, Panter KE, Pantaloni M, Spangenberger A, Harper JS. 149.  et al. 1999. The fetal cleft palate: II. Scarless healing after in utero repair of a congenital model. Plast. Reconstr. Surg. 104:1356–64 [Google Scholar]
  150. Kohl T, Tchatcheva K, Stressig R, Gembruch U, Kahl P. 150.  2009. Is there a therapeutic role for fetoscopic surgery in the prenatal treatment of gastroschisis? A feasibility study in sheep. Surg. Endosc. 23:1499–505 [Google Scholar]
/content/journals/10.1146/annurev-animal-030117-014637
Loading
/content/journals/10.1146/annurev-animal-030117-014637
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error