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The Future of Fetal Surgery

  • Eric Bergh
    Correspondence
    Corresponding author.
    Affiliations
    Department of Obstetrics and Gynecology, The Fetal Center at Children’s Memorial Hermann Hospital, University of Texas Health Science Center, McGovern Medical School, 6410 Fannin Street, Suite 700, Houston, TX 77030, USA
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  • Cara Buskmiller
    Affiliations
    Maternal Fetal Medicine, Department of Obstetrics and Gynecology, University of Texas Health Science Center, McGovern Medical School, 6410 Fannin Street, Suite 700, Houston, TX 77030, USA
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  • Anthony Johnson
    Affiliations
    Department of Obstetrics and Gynecology, The Fetal Center at Children’s Memorial Hermann Hospital, University of Texas Health Science Center, McGovern Medical School, 6410 Fannin Street, Suite 700, Houston, TX 77030, USA
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      References

        • Liley A.W.
        The use of amniocentesis and fetal transfusion in erythroblastosis fetalis.
        Pediatrics. 1965; 35: 836-847
        • Elias S.
        • Verp M.S.
        Prenatal diagnosis of genetic disorders.
        Obstet Gynecol Annu. 1983; 12: 79-102
        • Gohari P.
        • Spinelli A.
        Fetoscopy in the practice of perinatology and obstetrics.
        Obstet Gynecol Annu. 1979; 8: 179-202
        • Benzie R.J.
        • Doran T.A.
        The "fetoscope"--a new clinical tool for prenatal genetic diagnosis.
        Am J Obstet Gynecol. 1975; 121: 460-464
      1. First fetal surgery survivor finally meets his doctor.
        (Available at:) (Accessed March 5 2021)
        • Koehler S.M.
        • Knezevich M.
        • Wagner A.
        The evolution of fetal surgery.
        J Fetal Surg. 2017; 1: 7-23
        • Harrison M.R.
        • Filly R.A.
        • Golbus M.S.
        • et al.
        Fetal treatment 1982.
        N Engl J Med. 1982; 307: 1651-1652
        • Slaghekke F.
        • Lopriore E.
        • Lewi L.
        • et al.
        Fetoscopic laser coagulation of the vascular equator versus selective coagulation for twin-to-twin transfusion syndrome: an open-label randomised controlled trial.
        Lancet. 2014; 383: 2144-2151
        • Morris R.K.
        • Malin G.L.
        • Quinlan-Jones E.
        • et al.
        Percutaneous vesicoamniotic shunting versus conservative management for fetal lower urinary tract obstruction (PLUTO): a randomised trial.
        Lancet. 2013; 382: 1496-1506
        • Adzick N.S.
        • Thom E.A.
        • Spong C.Y.
        • et al.
        A randomized trial of prenatal versus postnatal repair of myelomeningocele.
        N Engl J Med. 2011; 364: 993-1004
        • Farrell J.
        • Howell L.J.
        An overview of surgical techniques, research trials, and future directions of fetal therapy.
        J Obstet Gynecol neonatal Nurs. 2012; 41: 419-425
        • Flake A.W.
        Surgery in the human fetus: the future.
        J Physiol. 2003; 547: 45-51
        • Harrison M.R.
        Fetal surgery: trials, tribulations, and turf.
        J Pediatr Surg. 2003; 38: 275-282
        • Deprest J.
        • Gratacos E.
        • Nicolaides K.H.
        • et al.
        Fetoscopic tracheal occlusion (FETO) for severe congenital diaphragmatic hernia: evolution of a technique and preliminary results.
        Ultrasound Obstet Gynecol. 2004; 24: 121-126
        • Sacco A.
        • Van der Veeken L.
        • Bagshaw E.
        • et al.
        Maternal complications following open and fetoscopic fetal surgery: a systematic review and meta-analysis.
        Prenat Diagn. 2019; 39: 251-268
        • Wenstrom K.D.
        • Carr S.R.
        Fetal surgery: principles, indications, and evidence.
        Obstet Gynecol. 2014; 124: 817-835
        • Sharma D.
        • Tsibizova V.I.
        Current perspective and scope of fetal therapy: part 1.
        J Matern Fetal Neonatal Med. 2020; : 1-29https://doi.org/10.1080/14767058.2020.1839880
        • Yamamoto M.
        • El Murr L.
        • Robyr R.
        • et al.
        Incidence and impact of perioperative complications in 175 fetoscopy-guided laser coagulations of chorionic plate anastomoses in fetofetal transfusion syndrome before 26 weeks of gestation.
        Am J Obstet Gynecol. 2005; 193: 1110-1116
        • Snowise S.
        • Mann L.K.
        • Moise Jr., K.J.
        • et al.
        Preterm prelabor rupture of membranes after fetoscopic laser surgery for twin-twin transfusion syndrome.
        Ultrasound Obstet Gynecol. 2017; 49: 607-611
        • Stirnemann J.
        • Djaafri F.
        • Kim A.
        • et al.
        Preterm premature rupture of membranes is a collateral effect of improvement in perinatal outcomes following fetoscopic coagulation of chorionic vessels for twin-twin transfusion syndrome: a retrospective observational study of 1092 cases.
        BJOG. 2018; 125: 1154-1162
        • Gratacos E.
        • Sanin-Blair J.
        • Lewi L.
        • et al.
        A histological study of fetoscopic membrane defects to document membrane healing.
        Placenta. 2006; 27: 452-456
        • Papanna R.
        • Bebbington M.W.
        • Moise Jr., K.
        Novel findings of iatrogenic fetal membrane defect after previous fetoscopy for twin-twin transfusion syndrome.
        Ultrasound Obstet Gynecol. 2013; 42: 118-119
        • Papanna R.
        • Mann L.K.
        • Johnson A.
        • et al.
        Chorioamnion separation as a risk for preterm premature rupture of membranes after laser therapy for twin-twin transfusion syndrome.
        Obstet Gynecol. 2010; 115: 771-776
        • Kohl T.
        Iatrogenic fetal membrane damage from complex fetoscopic surgery in human fetuses might not be amenable to simple closure by collagen plugs.
        Prenat Diagn. 2008; 28 ([author reply: 8–80]): 876-877
        • Belfort M.A.
        • Whitehead W.E.
        • Shamshirsaz A.A.
        • et al.
        Fetoscopic open neural tube defect repair: development and refinement of a two-port, carbon dioxide insufflation technique.
        Obstet Gynecol. 2017; 129: 734-743
        • Deprest J.A.
        • Van Schoubroeck D.
        • Van Ballaer P.P.
        • et al.
        Alternative technique for Nd:YAG laser coagulation in twin-to-twin transfusion syndrome with anterior placenta.
        Ultrasound Obstet Gynecol. 1998; 11: 347-352
        • Papanna R.
        • Molina S.
        • Moise K.Y.
        • et al.
        Chorioamnion plugging and the risk of preterm premature rupture of membranes after laser surgery in twin-twin transfusion syndrome.
        Ultrasound Obstet Gynecol. 2010; 35: 337-343
        • Chang J.
        • Tracy Jr., T.F.
        • Carr S.R.
        • et al.
        Port insertion and removal techniques to minimize premature rupture of the membranes in endoscopic fetal surgery.
        J Pediatr Surg. 2006; 41: 905-909
        • Luks F.I.
        • Deprest J.A.
        • Peers K.H.
        • et al.
        Gelatin sponge plug to seal fetoscopy port sites: technique in ovine and primate models.
        Am J Obstet Gynecol. 1999; 181: 995-996
        • Reddy U.M.
        • Shah S.S.
        • Nemiroff R.L.
        • et al.
        In vitro sealing of punctured fetal membranes: potential treatment for midtrimester premature rupture of membranes.
        Am J Obstet Gynecol. 2001; 185: 1090-1093
        • Papanna R.
        • Mann L.K.
        • Moise K.Y.
        • et al.
        Absorbable gelatin plug does not prevent iatrogenic preterm premature rupture of membranes after fetoscopic laser surgery for twin-twin transfusion syndrome.
        Ultrasound Obstet Gynecol. 2013; 42: 456-460
        • Bilic G.
        • Brubaker C.
        • Messersmith P.B.
        • et al.
        Injectable candidate sealants for fetal membrane repair: bonding and toxicity in vitro.
        Am J Obstet Gynecol. 2010; 202: 85.e1-9
        • Haller C.M.
        • Buerzle W.
        • Kivelio A.
        • et al.
        Mussel-mimetic tissue adhesive for fetal membrane repair: an ex vivo evaluation.
        Acta Biomater. 2012; 8: 4365-4370
        • Kivelio A.
        • Dekoninck P.
        • Perrini M.
        • et al.
        Mussel mimetic tissue adhesive for fetal membrane repair: initial in vivo investigation in rabbits.
        Eur J Obstet Gynecol Reprod Biol. 2013; 171: 240-245
        • Devaud Y.R.
        • Zuger S.
        • Zimmermann R.
        • et al.
        Minimally invasive surgical device for precise application of bioadhesives to prevent iPPROM.
        Fetal Diagn Ther. 2019; 45: 102-110
        • Micheletti T.
        • Eixarch E.
        • Berdun S.
        • et al.
        Ex-vivo mechanical sealing properties and toxicity of a bioadhesive patch as sealing system for fetal membrane iatrogenic defects.
        Sci Rep. 2020; 10: 18608
        • Kosa G.
        • Jakab P.
        • Szekely G.
        • et al.
        MRI driven magnetic microswimmers.
        Biomed Microdevices. 2012; 14: 165-178
        • Kohl T.
        • Hartlage M.G.
        • Kiehitz D.
        • et al.
        Percutaneous fetoscopic patch coverage of experimental lumbosacral full-thickness skin lesions in sheep.
        Surg Endosc. 2003; 17: 1218-1223
        • Aaronson O.S.
        • Tulipan N.B.
        • Cywes R.
        • et al.
        Robot-assisted endoscopic intrauterine myelomeningocele repair: a feasibility study.
        Pediatr Neurosurg. 2002; 36: 85-89
        • Berris M.
        • Shoham M.
        Febotics - a marriage of fetal surgery and robotics.
        Comput Aided Surg. 2006; 11: 175-180
        • Knight C.G.
        • Lorincz A.
        • Johnson A.
        • et al.
        Robot-enhanced fetoscopic surgery.
        J Pediatr Surg. 2004; 39: 1463-1465
        • Li J.
        • Esteban-Fernandez de Avila B.
        • Gao W.
        • et al.
        Micro/nanorobots for biomedicine: delivery, surgery, sensing, and detoxification.
        Sci Robot. 2017; 2 (eaam6431)
      2. Boswell T. Robotic fetal surgery: the next frontier? Available at: https://link.springer.com/chapter/10.1007%2F978-3-030-57219-8_25.

        • Nikitichev D.I.
        • Shakir D.I.
        • Chadebecq F.
        • et al.
        Medical-grade sterilizable target for fluid-immersed fetoscope optical distortion calibration.
        J Vis Exp. 2017; : 55298
        • Witt R.
        • MacKenzie T.C.
        • Peranteau W.H.
        Fetal stem cell and gene therapy.
        Semin Fetal Neonatal Med. 2017; 22: 410-414
        • Owen R.
        Immunogenic consequences of vascular anastomoses between bovine twins.
        Science. 1945; 102: 400-401
        • Billingham R.E.
        • Brent L.
        • Medawar P.B.
        ‘Actively acquired tolerance’ of foreign cells.
        Nature. 1953; 172: 603-606
        • Fleischman R.A.
        • Mintz B.
        Prevention of genetic anemias in mice by microinjection of normal hematopoietic stem cells into the fetal placenta.
        Proc Natl Acad Sci. 1979; 76: 5736-5740
        • Fleischman R.A.
        • Mintz B.
        Development of adult bone marrow stem cells in H-2-compatible and -incompatible mouse fetuses.
        J Exp Med. 1984; 159: 731-745
        • Peranteau W.H.
        • Hayashi S.
        • Hsieh M.
        • et al.
        High-level allogeneic chimerism achieved by prenatal tolerance induction and postnatal nonmyeloablative bone marrow transplantation.
        Blood. 2002; 100: 2225-2234
        • Nijagal A.
        • Derderian C.
        • Le T.
        • et al.
        Direct and indirect antigen presentation lead to deletion of donor-specific T cells after in utero hematopoietic cell transplantation in mice.
        Blood. 2013; 121: 4595-4602
        • Touraine J.L.
        • Raudrant D.
        • Royo C.
        • et al.
        In-utero transplantation of stem cells in bare lymphocyte syndrome.
        Lancet. 1989; 1: 1382
        • Flake A.W.
        • Roncarolo M.G.
        • Puck J.M.
        • et al.
        Treatment of X-linked severe combined immunodeficiency by in utero transplantation of paternal bone marrow.
        N Engl J Med. 1996; 335: 1806-1810
        • Wengler G.S.
        • Lanfranchi A.
        • Frusca T.
        • et al.
        In-utero transplantation of parental CD34 haematopoietic progenitor cells in a patient with X-linked severe combined immunodeficiency (SCIDXI).
        Lancet. 1996; 348: 1484-1487
        • Tiblad E.
        • Westgren M.
        Fetal stem-cell transplantation.
        Best Pract Res Clin Obstet Gynaecol. 2008; 22: 189-201
        • Weiss K.
        • Gonzalez A.
        • Lopez G.
        • et al.
        The clinical management of Type 2 Gaucher disease.
        Mol Genet Metab. 2015; 114: 110-122
        • Le Blanc K.
        • Gotherstrom C.
        • Ringden O.
        • et al.
        Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta.
        Transplantation. 2005; 79: 1607-1614
        • Palanki R.
        • Peranteau W.H.
        • Mitchell M.J.
        Delivery technologies for in utero gene therapy.
        Adv Drug Deliv Rev. 2020; 169: 51-62
        • Gotherstrom C.
        • Westgren M.
        • Shaw S.W.
        • et al.
        Pre- and postnatal transplantation of fetal mesenchymal stem cells in osteogenesis imperfecta: a two-center experience.
        Stem Cells Transl Med. 2014; 3: 255-264
        • Galganski L.A.
        • Kumar P.
        • Vanover M.A.
        • et al.
        In utero treatment of myelomeningocele with placental mesenchymal stromal cells - Selection of an optimal cell line in preparation for clinical trials.
        J Pediatr Surg. 2020; 55: 1941-1946
        • Kunisaki S.M.
        • Fuchs J.R.
        • Kaviani A.
        • et al.
        Diaphragmatic repair through fetal tissue engineering: a comparison between mesenchymal amniocyte- and myoblast-based constructs.
        J Pediatr Surg. 2006; 41 ([discussion: -9]): 34-39
        • Fuchs J.R.
        • Hannouche D.
        • Terada S.
        • et al.
        Fetal tracheal augmentation with cartilage engineered from bone marrow-derived mesenchymal progenitor cells.
        J Pediatr Surg. 2003; 38: 984-987
        • Fuchs J.R.
        • Terada S.
        • Ochoa E.R.
        • et al.
        Fetal tissue engineering: in utero tracheal augmentation in an ovine model.
        J Pediatr Surg. 2002; 37 ([discussion: -6]): 1000-1006
        • Peranteau W.H.
        • Endo M.
        • Adibe O.O.
        • et al.
        Evidence for an immune barrier after in utero hematopoietic-cell transplantation.
        Blood. 2007; 109: 1331-1333
        • Durkin E.T.
        • Jones K.A.
        • Rajesh D.
        • et al.
        Early chimerism threshold predicts sustained engraftment and NK-cell tolerance in prenatal allogeneic chimeras.
        Blood. 2008; 112: 5245-5253
        • Nijagal A.
        • Wegorzewska M.
        • Jarvis E.
        • et al.
        Maternal T cells limit engraftment after in utero hematopoietic cell transplantation in mice.
        J Clin Invest. 2011; 121: 582-592
        • Merianos D.J.
        • Tiblad E.
        • Santore M.T.
        • et al.
        Maternal alloantibodies induce a postnatal immune response that limits engraftment following in utero hematopoietic cell transplantation in mice.
        J Clin Invest. 2009; 119: 2590-2600
        • Stitelman D.H.
        • Brazelton T.
        • Bora A.
        • et al.
        Developmental stage determines efficiency of gene transfer to muscle satellite cells by in utero delivery of adeno-associated virus vector serotype 2/9.
        Mol Ther Methods Clin Dev. 2014; 1: 14040
        • Endo M.
        • Henriques-Coelho T.
        • Zoltick P.W.
        • et al.
        The developmental stage determines the distribution and duration of gene expression after early intra-amniotic gene transfer using lentiviral vectors.
        Gene Ther. 2010; 17: 61-71
        • Joyeux L.
        • Danzer E.
        • Limberis M.P.
        • et al.
        In utero lung gene transfer using adeno-associated viral and lentiviral vectors in mice.
        Hum Gene Ther Methods. 2014; 25: 197-205
        • Sabatino D.E.
        • Mackenzie T.C.
        • Peranteau W.
        • et al.
        Persistent expression of hF.IX after tolerance induction by in utero or neonatal administration of AAV-1-F.IX in hemophilia B mice.
        Mol Ther. 2007; 15: 1677-1685
        • Roybal J.L.
        • Endo M.
        • Radu A.
        • et al.
        Early gestational gene transfer with targeted ATP7B expression in the liver improves phenotype in a murine model of Wilson's disease.
        Gene Ther. 2012; 19: 1085-1094
        • Koppanati B.M.
        • Li J.
        • Xiao X.
        • et al.
        Systemic delivery of AAV8 in utero results in gene expression in diaphragm and limb muscle: treatment implications for muscle disorders.
        Gene Ther. 2009; 16: 1130-1137
        • George L.A.
        • Fogarty P.F.
        Gene therapy for hemophilia: past, present and future.
        Semin Hematol. 2016; 53: 46-54
        • Calcedo R.
        • Griesenbach U.
        • Dorgan D.J.
        • et al.
        Self-reactive CFTR T cells in humans: implications for gene therapy.
        Hum Gene Ther Clin Dev. 2013; 24: 108-115
        • Mingozzi F.
        • Maus M.V.
        • Hui D.J.
        • et al.
        CD8+ T-cell responses to adeno-associated virus capsid in humans.
        Nat Med. 2007; 13: 419-422
        • Davey M.G.
        • Riley J.S.
        • Andrews A.
        • et al.
        Induction of immune tolerance to foreign protein via adeno-associated viral vector gene transfer in mid-gestation fetal sheep.
        PLoS One. 2017; 12: e0171132
        • Calcedo R.
        • Morizono H.
        • Wang L.
        • et al.
        Adeno-associated virus antibody profiles in newborns, children, and adolescents.
        Clin Vaccin Immunol. 2011; 18: 1586-1588
        • Maeder M.L.
        • Gersbach C.A.
        Genome-editing technologies for gene and cell therapy.
        Mol Ther. 2016; 24: 430-446
        • Yang Y.
        • Wang L.
        • Bell P.
        • et al.
        A dual AAV system enables the Cas9-mediated correction of a metabolic liver disease in newborn mice.
        Nat Biotechnol. 2016; 34: 334-338
        • Tabebordbar M.
        • Zhu K.
        • Cheng J.K.W.
        • et al.
        In vivo gene editing in dystrophic mouse muscle and muscle stem cells.
        Science. 2016; 351: 407-411
        • Usuda H.
        • Watanabe S.
        • Saito M.
        • et al.
        Successful use of an artificial placenta to support extremely preterm ovine fetuses at the border of viability.
        Am J Obstet Gynecol. 2019; 221: 69 e1-e17
        • Stoll B.J.
        • Hansen N.I.
        • Bell E.F.
        • et al.
        Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993-2012.
        JAMA. 2015; 314: 1039-1051
        • Stoinska B.
        • Gadzinowski J.
        Neurological and developmental disabilities in ELBW and VLBW: follow-up at 2 years of age.
        J Perinatol. 2011; 31: 137-142
        • Stoll B.J.
        • Hansen N.I.
        • Bell E.F.
        • et al.
        Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network.
        Pediatrics. 2010; 126: 443-456
        • Brumbaugh J.E.
        • Hansen N.I.
        • Bell E.F.
        • et al.
        Outcomes of extremely preterm infants with birth weight less than 400 g.
        JAMA Pediatr. 2019; 173: 434-445
        • Anderson J.G.
        • Baer R.J.
        • Partridge J.C.
        • et al.
        Survival and major morbidity of extremely preterm infants: a population-based study.
        Pediatrics. 2016; 138: e20154434
        • Partridge E.A.
        • Davey M.G.
        • Hornick M.A.
        • et al.
        An extra-uterine system to physiologically support the extreme premature lamb.
        Nat Commun. 2017; 8: 15112
        • Sahoo T.
        • Gulla K.M.
        Artificial placenta: miles to go before I sleep.
        Am J Obstet Gynecol. 2019; 221: 368-369
        • Usuda H.
        • Watanabe S.
        • Saito M.
        • et al.
        Successful use of an artificial placenta-based life support system to treat extremely preterm ovine fetuses compromised by intrauterine inflammation.
        Am J Obstet Gynecol. 2020; 223: 755.e1-755.e20