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Mechanisms, Etiology, and Classification of Rare Clefts

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Facial Reconstruction of Unusual Facial Clefts

Abstract

Progresses in biology bring new understandings to the mechanisms of normal morphogenesis that, when everything goes well, yields normal people.

Going through embryology, histogenesis, genetics, and macromolecular is a journey toward more profound knowledge. More and more genetic dysfunctions, either due to mutations or environmental, are found to be related to malformations named rare clefts. Even whether precise sequences are not fully understood, when carefully looking at an extensive series of rare clefts either found in the literature or in a series as large as the one merged from two craniofacial centers with a huge caseload, we have the feeling that phenotypes including a rare cleft could, probably, be related to alterations, may be different, but occurring in a same genetic cascade. Tessier’s classification has been a significant step, in the twentieth century, in the science of those rare craniofacial malformations. Progresses in advanced medical imaging and genetics will allow a second major step in this way.

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References

  1. Hall BK. The neural crest in development and evolution. New York: Springer; 1999. https://doi.org/10.1007/978-1-4757-3064-7.

    Book  Google Scholar 

  2. Haeckel E. The evolution of man, vol. 1. London: Watts & Co; 1910. p. 351.

    Google Scholar 

  3. Depew MJ, Simpson CA. 21st Century neontology and the comparative development of the vertebrate skull. Dev Dyn. 2006;235(5):1256–91. https://doi.org/10.1002/dvdy.20796.

    Article  PubMed  Google Scholar 

  4. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head. Science. 1983;220(4594):268–73. https://doi.org/10.1126/science.220.4594.268.

    Article  CAS  PubMed  Google Scholar 

  5. De Beer GR. The development of the vertebrate skull. Oxford: Clarendon Press; 1937. p. 550.

    Google Scholar 

  6. Dias MS, Walker ML. The Embryogenesis of Complex Dysraphic Malformations: A Disorder of Gastrulation? Pediatr Neurosurg. 1992;18(5–6):229–53. https://www.karger.com/Article/FullText/120670.

    Article  CAS  PubMed  Google Scholar 

  7. Langman J, Sadler TW. Langman’s medical embryology. 6th ed. Baltimore: Williams and Wilkins; 1990. p. 409.

    Google Scholar 

  8. Agius E, Piccolo S, De Robertis EM. L’inducteur céphalique Cerberus est un inhibiteur multivalent extracellulaire. J Soc Biol. 1999;193(4–5):347–54. https://doi.org/10.1051/jbio/1999193040347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gur M, Edri T, Moody SA, Fainsod A. Retinoic acid is required for normal morphogenetic movements during gastrulation. Front Cell Dev Biol. 2022;10:857230. https://doi.org/10.3389/fcell.2022.857230/full.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Haworth KE, Healy C, Morgan P, Sharpe PT. Regionalisation of early head ectoderm is regulated by endoderm and prepatterns the orofacial epithelium. Development. 2004;131(19):4797–806. https://journals.biologists.com/dev/article/131/19/4797/42427/Regionalisation-of-early-head-ectoderm-is.

    Article  CAS  PubMed  Google Scholar 

  11. Le Douarin NM. The avian embryo as a model to study the development of the neural crest: a long and still ongoing story. Mech Dev. 2004;121(9):1089–102. https://linkinghub.elsevier.com/retrieve/pii/S0925477304001625.

    Article  PubMed  Google Scholar 

  12. His W. Untersuchungen über die erste Anlage des Wirbelthierleibes: die erste Entwickelung des Hühnchens im Ei [Internet]. Leipzig: F.C.W. Vogel; 1868. https://archive.org/details/b21993579/page/n288/mode/1up.

    Book  Google Scholar 

  13. Kuriyama S, Mayor R. Molecular analysis of neural crest migration. Philos Trans R Soc B Biol Sci. 2008;363(1495):1349–62. https://doi.org/10.1098/rstb.2007.2252.

    Article  Google Scholar 

  14. Abramyan J. Hedgehog signaling and embryonic craniofacial disorders. J Dev Biol. 2019;7(2):9. https://www.mdpi.com/2221-3759/7/2/9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Saadi I, Alkuraya FS, Gisselbrecht SS, Goessling W, Cavallesco R, Turbe-Doan A, et al. Deficiency of the cytoskeletal protein SPECC1L leads to oblique facial clefting. Am J Hum Genet. 2011;89(1):44–55. https://linkinghub.elsevier.com/retrieve/pii/S0002929711002163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kulesa PM, Bailey CM, Kasemeier-Kulesa JC, McLennan R. Cranial neural crest migration: new rules for an old road. Dev Biol. 2010;344(2):543–54. https://linkinghub.elsevier.com/retrieve/pii/S001216061000240X.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lim HYG, Plachta N. Cytoskeletal control of early mammalian development. Nat Rev Mol Cell Biol [Internet]. 2021;22(8):548–62. http://www.nature.com/articles/s41580-021-00363-9.

    Article  CAS  PubMed  Google Scholar 

  18. Blaue C, Kashef J, Franz CM. Cadherin-11 promotes neural crest cell spreading by reducing intracellular tension-mapping adhesion and mechanics in neural crest explants by atomic force microscopy. Semin Cell Dev Biol. 2018;73:95–106.

    Article  CAS  PubMed  Google Scholar 

  19. Andrieu C, Montigny A, Bibonne A, Despin-Guitard E, Alfandari D, Théveneau E. MMP14 is required for delamination of chick neural crest cells independently of its catalytic activity. Dev Camb Engl. 2020;147(7):dev183954.

    CAS  Google Scholar 

  20. McLennan R, Teddy JM, Kasemeier-Kulesa JC, Romine MH, Kulesa PM. Vascular endothelial growth factor (VEGF) regulates cranial neural crest migration in vivo. Dev Biol. 2010;339(1):114–25. https://linkinghub.elsevier.com/retrieve/pii/S0012160609014286.

    Article  CAS  PubMed  Google Scholar 

  21. Creuzet S, Schuler B, Couly G, Le Douarin NM. Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc Natl Acad Sci. 2004;101(14):4843–7. https://doi.org/10.1073/pnas.0400869101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Perris R, Perissinotto D. Role of the extracellular matrix during neural crest cell migration. Mech Dev. 2000;95(1):3–21. https://www.sciencedirect.com/science/article/pii/S0925477300003658.

    Article  CAS  PubMed  Google Scholar 

  23. Wedden SE. Morphogenesis of the head and face: discussion report. Dev Camb Engl. 1988;103(Suppl):61–2.

    Google Scholar 

  24. Thorogood P. Mechanisms of morphogenetic specification in skull development. In: Wolff JR, Sievers J, Berry M, eds. Mesenchymal-epithelial interactions in neural development. Springer Berlin Heidelberg; 1987:141–52. https://doi.org/10.1007/978-3-642-71837-3_12.

  25. Sato T, Kurihara Y, Asai R, Kawamura Y, Tonami K, Uchijima Y, et al. An endothelin-1 switch specifies maxillomandibular identity. Proc Natl Acad Sci. 2008;105(48):18806–11. https://doi.org/10.1073/pnas.0807345105.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Compagnucci C, Fish JL, Schwark M, Tarabykin V, Depew MJ. Pax6 regulates craniofacial form through its control of an essential cephalic ectodermal patterning center. Genesis. 2011;49(4):307–25. https://doi.org/10.1002/dvg.20724.

    Article  CAS  PubMed  Google Scholar 

  27. Depew MJ, Simpson CA, Morasso M, Rubenstein JLR. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J Anat 2005 207(5):501–561. https://doi.org/10.1111/j.1469-7580.2005.00487.x

  28. Hu D, Marcucio RS, Helms JA. A zone of frontonasal ectoderm regulates patterning and growth in the face. Development. 2003;130(9):1749–58. https://journals.biologists.com/dev/article/130/9/1749/52408/A-zone-of-frontonasal-ectoderm-regulates.

    Article  CAS  PubMed  Google Scholar 

  29. Griffin JN, Compagnucci C, Hu D, Fish J, Klein O, Marcucio R, et al. Fgf8 dosage determines midfacial integration and polarity within the nasal and optic capsules. Dev Biol. 2013;374(1):185–97. https://linkinghub.elsevier.com/retrieve/pii/S0012160612006331.

    Article  CAS  PubMed  Google Scholar 

  30. Le Douarin NM, Creuzet S, Couly G, Dupin E. Neural crest cell plasticity and its limits. Development. 2004;131(19):4637–50. https://journals.biologists.com/dev/article/131/19/4637/42419/Neural-crest-cell-plasticity-and-its-limits.

    Article  PubMed  Google Scholar 

  31. Young NM, Hu D, Lainoff AJ, Smith FJ, Diaz R, Tucker AS, et al. Embryonic bauplans and the developmental origins of facial diversity and constraint. Dev Camb Engl. 2014;141(5):1059–63. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3929406/.

    CAS  Google Scholar 

  32. Hu D, Young NM, Li X, Xu Y, Hallgrímsson B, Marcucio RS. A dynamic Shh expression pattern, regulated by SHH and BMP signaling, coordinates fusion of primordia in the amniote face. Dev Camb Engl. 2015;142(3):567–74.

    CAS  Google Scholar 

  33. Twigg SRF, Wilkie AOM. New insights into craniofacial malformations. Hum Mol Genet. 2015 24(R1):R50–R59. https://doi.org/10.1093/hmg/ddv228

  34. Kurosaka H, Iulianella A, Williams T, Trainor PA. Disrupting hedgehog and WNT signaling interactions promotes cleft lip pathogenesis. J Clin Invest. 2014;124(4):1660–71. http://www.jci.org/articles/view/72688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zaghloul NA, Brugmann SA. The emerging face of primary cilia. Genesis. 2011;49(4):231–46. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3118297/.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Huangfu D, Anderson KV. Cilia and hedgehog responsiveness in the mouse. Proc Natl Acad Sci U S A. 2005;102(32):11325–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Neugebauer JM, Amack JD, Peterson AG, Bisgrove BW, Yost HJ. FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature. 2009;458(7238):651–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Strutt D. The planar polarity pathway. Curr Biol. 2008;18(19):R898–902. https://linkinghub.elsevier.com/retrieve/pii/S0960982208009640.

    Article  CAS  PubMed  Google Scholar 

  39. Zhang Z, Wlodarczyk BJ, Niederreither K, Venugopalan S, Florez S, Finnell RH, et al. Fuz regulates craniofacial development through tissue specific responses to signaling factors. PLoS One. 2011;6(9):e24608. https://doi.org/10.1371/journal.pone.0024608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Liu B, Chen S, Johnson C, Helms JA. A ciliopathy with hydrocephalus, isolated craniosynostosis, hypertelorism, and clefting caused by deletion of Kif3a. Reprod Toxicol Elmsford N. 2014;48:88–97.

    Article  CAS  Google Scholar 

  41. Poswillo D. The pathogenesis of the first and second branchial arch syndrome. Oral Surg Oral Med Oral Pathol. 1973;35(3):302–28. https://linkinghub.elsevier.com/retrieve/pii/0030422073900704.

    Article  CAS  PubMed  Google Scholar 

  42. Poswillo D. The aetiology and pathogenesis of craniofacial deformity. Dev Camb Engl. 1988;103(Suppl):207–12.

    Google Scholar 

  43. Braithwaite F, Watson J. A report on three unusual cleft lips. Br J Plast Surg. 1949;2(1):38–49. https://linkinghub.elsevier.com/retrieve/pii/S0007122649800075.

    Article  CAS  PubMed  Google Scholar 

  44. Ribatti D. Genetic and epigenetic mechanisms in the early development of the vascular system. J Anat. 2006;208(2):139–52. https://doi.org/10.1111/j.1469-7580.2006.00522.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Aghi M, Chiocca EA. Contribution of bone marrow-derived cells to blood vessels in ischemic tissues and tumors. Mol Ther. 2005;12(6):994–1005. https://www.cell.com/molecular-therapy-family/molecular-therapy/abstract/S1525-0016(05)01431-0.

    Article  CAS  PubMed  Google Scholar 

  46. Ausprunk DH, Folkman J. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res. 1977;14(1):53–65. https://linkinghub.elsevier.com/retrieve/pii/0026286277901418.

    Article  CAS  PubMed  Google Scholar 

  47. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9(6):8.

    Article  Google Scholar 

  48. Finley EB. The development of the subcutaneous vascular plexus in the head of the human embryo. In: Contribution to embryology. Washington: Carnegie Institution; 1922. p. 155–61. https://archive.org/details/contributionstoe14carn/page/n191/mode/2up.

    Google Scholar 

  49. Hochstetter F. Über die Vaskularisation der Haut des Schädeldaches menschlicher Embryonen. Wien: Komm. A. Hölder; 1917.

    Google Scholar 

  50. Marcelo KL, Goldie LC, Hirschi KK. Regulation of endothelial cell differentiation and specification. Circ Res. 2013;112(9):1272–87. https://doi.org/10.1161/CIRCRESAHA.113.300506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Richman JM, Buchtová M, Boughner JC. Comparative ontogeny and phylogeny of the upper jaw skeleton in amniotes. 2006;235(Dev Dyn, 5):1230–43. https://doi.org/10.1002/dvdy.20716.

  52. Frohman MA, Boyle M, Martin GR. Isolation of the mouse Hox-2.9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development. 1990;110(2):589–607.

    Article  CAS  PubMed  Google Scholar 

  53. Spranger J, Benirschke K, Hall JG, Lenz W, Lowry RB. Errors of morphogenesis: concepts and terms. J Pediatr. 1982;1:6.

    Google Scholar 

  54. Sulik KK, Cook CS, Webster WS. Teratogens and craniofacial malformations: relationships to cell death. Development. 1988;103(Supplement):213–32. https://journals.biologists.com/dev/article/103/Supplement/213/36094/Teratogens-and-craniofacial-malformations.

    Article  CAS  PubMed  Google Scholar 

  55. Panoutsopoulos AA, De Crescenzo AH, Lee A, Lu AM, Ross AP, Borodinsky LN, et al. Pak1ip1 loss-of-function leads to cell cycle arrest, loss of neural crest cells, and craniofacial abnormalities. Front Cell Dev Biol. 2020;8:510063.

    Article  PubMed  PubMed Central  Google Scholar 

  56. van Boxtel AL, Pieterse B, Cenijn P, Kamstra JH, Brouwer A, van Wieringen W, et al. Dithiocarbamates induce craniofacial abnormalities and downregulate sox9a during zebrafish development. Toxicol Sci. 2010;117(1):209–17. https://doi.org/10.1093/toxsci/kfq169.

    Article  CAS  PubMed  Google Scholar 

  57. Obwegeser HL, Weber G, Freihofer HP, Sailer HF. Facial duplication—the unique case of Antonio. J Maxillofac Surg. 1978;6:179–98. https://linkinghub.elsevier.com/retrieve/pii/S0301050378800885.

    Article  CAS  PubMed  Google Scholar 

  58. Perea-Gomez A, Vella FDJ, Shawlot W, Oulad-Abdelghani M, Chazaud C, Meno C, et al. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell. 2002;3(5):745–56. https://linkinghub.elsevier.com/retrieve/pii/S1534580702003210.

    Article  CAS  PubMed  Google Scholar 

  59. O’Rahilly R, Müller F. Bidirectional closure of the rostral neuropore in the human embryo: closure of rostral neuropore. Am J Anat. 1989;184(4):259–68. https://doi.org/10.1002/aja.1001840402.

    Article  PubMed  Google Scholar 

  60. Fong KSK, Adachi DAT, Chang SB, Lozanoff S. Midline craniofacial malformations with a lipomatous cephalocele are associated with insufficient closure of the neural tube in the tuft mouse. Birth Defects Res A Clin Mol Teratol. 2014;100(8):598–607. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4426337/.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Quaderi NA, Schweiger S, Gaudenz K, Franco B, Rugarli EI, Berger W, et al. Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nat Genet [Internet]. 1997;17(3):285–91. http://www.nature.com/articles/ng1197-285.

    Article  CAS  PubMed  Google Scholar 

  62. Calo E, Gu B, Bowen ME, Aryan F, Zalc A, Liang J, et al. Tissue-selective effects of nucleolar stress and rDNA damage in developmental disorders. Nature. 2018;554(7690):112–7. http://www.nature.com/articles/nature25449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Gfrerer L, Shubinets V, Hoyos T, Kong Y, Nguyen C, Pietschmann P, et al. Functional analysis of SPECC1L in craniofacial development and oblique facial cleft pathogenesis. Plast Reconstr Surg. 2014;134(4):748–59. http://journals.lww.com/00006534-201410000-00032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Twigg SRF, Versnel SL, Nürnberg G, Lees MM, Bhat M, Hammond P, et al. Frontorhiny, a distinctive presentation of frontonasal dysplasia caused by recessive mutations in the ALX3 homeobox gene. Am J Hum Genet. 2009;84(5):698–705. https://linkinghub.elsevier.com/retrieve/pii/S0002929709001517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Uz E, Alanay Y, Aktas D, Vargel I, Gucer S, Tuncbilek G, et al. Disruption of ALX1 causes extreme microphthalmia and severe facial clefting: expanding the spectrum of autosomal-recessive ALX-related frontonasal dysplasia. Am J Hum Genet. 2010;86(5):789–96. https://linkinghub.elsevier.com/retrieve/pii/S000292971000203X.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Dee CT, Szymoniuk CR, Mills PED, Takahashi T. Defective neural crest migration revealed by a zebrafish model of Alx1-related frontonasal dysplasia. Hum Mol Genet. 2013;22(2):239–51.

    Article  CAS  PubMed  Google Scholar 

  67. Smith JD, Hing AV, Clarke CM, Johnson NM, Perez FA, Park SS, et al. Exome sequencing identifies a recurrent De novo ZSWIM6 mutation associated with acromelic frontonasal dysostosis. Am J Hum Genet. 2014;95(2):235–40. https://linkinghub.elsevier.com/retrieve/pii/S0002929714003176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Twigg SRF, Ousager LB, Miller KA, Zhou Y, Elalaoui SC, Sefiani A, Bak GS, Hove H, Hansen LK, Fagerberg CR, Tajir M, Wilkie AOM. Acromelic frontonasal dysostosis and ZSWIM6 mutation: phenotypic spectrum and mosaicism. Clin Genet. 2016;90(3):270–5. https://doi.org/10.1111/cge.12721.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lehalle D, Altunoglu U, Bruel AL, Arnaud E, Blanchet P, Choi JW, et al. Clinical delineation of a subtype of frontonasal dysplasia with creased nasal ridge and upper limb anomalies: report of six unrelated patients. Am J Med Genet A. 2017;173(12):3136–42. https://doi.org/10.1002/ajmg.a.38490.

    Article  CAS  PubMed  Google Scholar 

  70. Hufnagel RB, Zimmerman SL, Krueger LA, Bender PL, Ahmed ZM, Saal HM. A new frontonasal dysplasia syndrome associated with deletion of the SIX2 gene. Am J Med Genet A. 2016;170A(2):487–91. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8108007/

    Article  PubMed  Google Scholar 

  71. Ross W. A curious monster which lived for some time after birth. Trans Obstet Soc Lond. 1867;IX:31–2.

    Google Scholar 

  72. Chavane A. Malformation faciale (section par bride amniotique). Bull Société Anat Paris. 1890;5(4):137–41. https://gallica.bnf.fr/ark:/12148/bpt6k6327302h/f159.item#.

    Google Scholar 

  73. Marchand F. Missbildungen. In: Eulenburg A, editor. Real-encyclopädie der gesammten heilkunde: medicinisch-chirurgisches handworterbuch fu˝r praktische aerzte. Wien: Urban and Schwarzenberg; 1897. p. 423–596.

    Google Scholar 

  74. Opitz JM, Johnson DR, Gilbert-Barness EF. ADAM “sequence” part II: hypothesis and speculation. Am J Med Genet A. 2015;167(3):478–503. https://doi.org/10.1002/ajmg.a.36937.

    Article  CAS  Google Scholar 

  75. Ballantyne JW. Spontaneous or congenital amputations. In: Manual of antenatal pathology and hygiene. Edinburgh: William Green & sons; 1902. p. 396–7. http://www.archive.org/details/manualofantenata00ballrich.

    Google Scholar 

  76. Jones KL, Smith DW, Hall BD, Hall JG, Ebbin AJ, Massoud H, et al. A pattern of craniofacial and limb defects secondary to aberrant tissue bands. J Pediatr. 1974;84(1):90–5. https://linkinghub.elsevier.com/retrieve/pii/S0022347674805597.

    Article  CAS  PubMed  Google Scholar 

  77. Higginbottom MC, Jones KL, Hall BD, Smith DW. The amniotic band disruption complex: timing of amniotic rupture and variable spectra of consequent defects. J Pediatr. 1979;95(4):544–9.

    Article  CAS  PubMed  Google Scholar 

  78. Torpin R. Amniochorionic mesoblastic fibrous strings and amnionic bands. Am J Obstet Gynecol. 1965;91(1):65–75. https://linkinghub.elsevier.com/retrieve/pii/0002937865905880.

    Article  CAS  PubMed  Google Scholar 

  79. Bamforth JS. Amniotic band sequence: Streeter’s hypothesis reexamined. Am J Med Genet. 1992;44(3):280–7. https://doi.org/10.1002/ajmg.1320440304.

    Article  CAS  PubMed  Google Scholar 

  80. Keith A. Concerning the origin and nature of certain malformations of the face, head, and foot. Br J Surg. 2005;28(110):173–92. https://academic.oup.com/bjs/article/28/110/173/6222774.

    Article  Google Scholar 

  81. Van Allen MI, Curry C, Gallagher L, Reynolds JF. Limb body wall complex: I. Pathogenesis. Am J Med Genet. 1987;28(3):529–48. https://doi.org/10.1002/ajmg.1320280302.

    Article  PubMed  Google Scholar 

  82. Hunter AGW, Carpenter BF, Opitz JM, Reynolds JF. Implications of malformations not due to amniotic bands in the amniotic band sequence. Am J Med Genet. 1986;24(4):691–700. https://doi.org/10.1002/ajmg.1320240414.

    Article  CAS  PubMed  Google Scholar 

  83. Bagg HJ. Hereditary abnormalities of the limbs, their origin and transmission. II. A morphological study with special reference to the etiology of club-feet, syndactylism, hypodactylism, and congenital amputation in the descendants of X-rayed mice. Am J Anat. 1929;43(2):167–219. https://doi.org/10.1002/aja.1000430203.

    Article  Google Scholar 

  84. Hummel KP. The inheritance and expression of disorganization, an unusual mutation in the mouse. J Exp Zool. 1958;137(3):389–423. https://doi.org/10.1002/jez.1401370303.

    Article  CAS  PubMed  Google Scholar 

  85. Donnai D, Winter RM. Disorganisation: a model for ‘early amnion rupture’? J Med Genet. 1989;26(7):421–5. https://doi.org/10.1136/jmg.26.7.421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Purandare SM, Ernst L, Medne L, Huff D, Zackai EH. Developmental anomalies with features of disorganization (Ds) and amniotic band sequence (ABS): a report of four cases. Am J Med Genet A. 2009;149A(8):1740–8. https://doi.org/10.1002/ajmg.a.32716.

    Article  PubMed  Google Scholar 

  87. Lowry RB, Yong SL. Cleft lip and palate, sensorineural deafness, and sacral lipoma in two brothers: a possible example of the disorganisation mutant. J Med Genet. 1991;28(2):135–7. https://doi.org/10.1136/jmg.28.2.135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Lin AE. Two additional patients representing the possible human homologue for the mouse mutant disorganisation (ds). J Med Genet. 1991;28(9):645–7. https://jmg.bmj.com/lookup/doi/10.1136/jmg.28.9.645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Crosby JL, Varnum DS, Washburn LL, Nadeau JH. Disorganization is a completely dominant gain-of-function mouse mutation causing sporadic developmental defects. Mech Dev. 1992;37(3):121–6. https://linkinghub.elsevier.com/retrieve/pii/092547739290074T.

    Article  CAS  PubMed  Google Scholar 

  90. De Michelena MI, Stachurska A. Multiple anomalies possibly caused by a human homologue to the mouse disorganization (Ds) gene. Clin Dysmorphol. 1993;2(2):131–4. https://journals.lww.com/clindysmorphol/Abstract/1993/04000/Multiple_anomalies_possibly_caused_by_a_human.6.aspx.

    Article  PubMed  Google Scholar 

  91. Elliott AM, Chen MF, Azouz EM, Teebi AS. Developmental anomalies suggestive of the human homologue of the mouse mutant disorganization. Am J Med Genet. 1995;55(2):240–3. https://doi.org/10.1002/ajmg.1320550218.

    Article  CAS  PubMed  Google Scholar 

  92. Teebi AS, Elliott AM. Another case of the human homologue of the mouse mutant disorganization. Am J Med Genet. 1996;61(1):94.

    Article  CAS  PubMed  Google Scholar 

  93. Van Langen IM, Hennekam RCM. Another example of the human homologue of the mouse mutant disorganization? Clin Dysmorphol. 1994;3(4):361–2. https://journals.lww.com/clindysmorphol/Citation/1994/10000/Another_example_of_the_human_homologue_of_the.15.aspx.

    PubMed  Google Scholar 

  94. Robin NH, Nadeau JH. Disorganization in mice and humans. Am J Med Genet. 2001;101(4):334–8. https://doi.org/10.1002/1096-8628(20010715)101:4<334::AID-AJMG1233>3.0.CO;2-7.

    Article  CAS  PubMed  Google Scholar 

  95. Korniszewski L, Skorka A, Donnai D. Disorganisation: a case with popliteal pterygia and placental-skin appendages. Clin Dysmorphol. 1999;8(4):277–81.

    Article  CAS  PubMed  Google Scholar 

  96. Delgado Luengo WN, Luisa Hernández Rodríguez M, Valbuena Pirela I, González Ferrer S, Estrada Corona P, Chacón Fonseca I, et al. Human disorganization complex, as a polytopic blastogenesis defect: a new case: human disorganization and blastogenesis defect. Am J Med Genet A. 2004;125A(2):181–5. https://doi.org/10.1002/ajmg.a.20307.

    Article  PubMed  Google Scholar 

  97. O’Driscoll M, Peckham C, Kerr B. Four limb syndactyly, constriction rings and skin tags; amniotic bands or disorganization-like syndrome. Clin Dysmorphol. 2008;17(4):255–8. https://journals.lww.com/clindysmorphol/Abstract/2008/10000/Four_limb_syndactyly,_constriction_rings_and_skin.4.aspx.

    Article  PubMed  Google Scholar 

  98. Vallejo OG, Benítez Sánchez Mdel C, Cánovas CS, Ontiveros JD, Ruiz Jiménez JI, Bermejo-Sánchez E, et al. Patient with disorganization syndrome: Surgical procedures, Pathology, and potential causes: patient with disorganization syndrome. Birth Defects Res A Clin Mol Teratol. 2013;97(12):781–5. https://doi.org/10.1002/bdra.23203.

    Article  CAS  PubMed  Google Scholar 

  99. Crosby JL, Varnum DS, Nadeau JH. Two-hit model for sporadic congenital anomalies in mice with the disorganization mutation. Am J Hum Genet. 1993;52(5):866–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Isidor B, Baujat G, Le Caignec C, Pichon O, Martin-Coignard D, Toutain A, et al. Congenital skin pedicles with or without amniotic band sequence: extending the human phenotype resembling mouse disorganization. Am J Med Genet A. 2009;149A(8):1734–9. https://doi.org/10.1002/ajmg.a.32796.

    Article  CAS  PubMed  Google Scholar 

  101. White RA, Dowler LL, Pasztor LM, Gatson LL, Adkison LR, Angeloni SV, et al. Assignment of the transcription factor GATA4 gene to human chromosome 8 and mouse chromosome 14: Gata4 is a candidate gene for ds (disorganization). Genomics. 1995;27(1):20–6. https://linkinghub.elsevier.com/retrieve/pii/S0888754385710038.

    Article  CAS  PubMed  Google Scholar 

  102. Huang WY, HHQ H, Liew CC. Assignment of the human GATA4 gene to 8p23.1-->p22 using fluorescence in situ hybridization analysis. Cytogenet Genome Res. 1996;72(2–3):217–8. https://www.karger.com/Article/FullText/134194.

    Article  CAS  Google Scholar 

  103. Kruszka P, Uwineza A, Mutesa L, Martinez AF, Abe Y, Zackai EH, et al. Limb body wall complex, amniotic band sequence, or new syndrome caused by mutation in IQ Motif containing K (IQCK)? Mol Genet Genomic Med. 2015;3(5):424–32. https://doi.org/10.1002/mgg3.153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Geoffroy Saint Hilaire I. Histoire générale et particuliére des anomalies de l’organisation chez l’homme et les animaux. Paris: Bailliére; 1837. https://ia800106.us.archive.org/17/items/BIUSante_35541/BIUSante_35541.pdf.

    Google Scholar 

  105. Dick W. Case of Hyperencephalous monstrosity. Lond Med Gaz. 1837;19:897–9. https://archive.org/details/londonmedicalgaz19londuoft/page/898/mode/2up.

    Google Scholar 

  106. Guersant. presentation de malade. Gaz Hôp Civ Mil Lancette Fr 1860 33 (30 pp112 et N° 31 pp 119(fig.)):112. http://www.biusante.parisdescartes.fr/histmed/medica/cote?90130x1860

  107. Butcher H. Reports in operative surgery. Dublin Quaterly J Med Sci. 1860;XXIX:258.

    Google Scholar 

  108. Fergusson W. A system of practical surgery. 5th ed. London: John Churchill and sons; 1870. p. 812. http://www.archive.org/details/5thsystemofpract00ferguoft.

    Google Scholar 

  109. Dupuy LE. Anormalité congénitale du globe oculaire chez un fœtus atteint également d’hydrocéphalie, de bec-de-lièvre et de syndactylie des pieds et des mains. Bull Société Anat Paris. 1874:12–4.

    Google Scholar 

  110. Debout. Coup d’oeil sur une des formes les plus rares du bec de liévre, les fissures horizontales. Remarques et observations. Bull Général Thérapeutique Médicale Chir. 1862;(N 63):13–22. https://services.biusante.parisdescartes.fr/medica-pdf/main.php?key=cGFydGlhbHw5MDAxNHgxODYyeDYzfDEyfDIz.

  111. Pelvet. Mémoire sur les fissures congénitales des joues; lu à la société de biologie. Gaz Médicale Paris. 2022;3(N 19):418–22. https://services.biusante.parisdescartes.fr/medica-pdf/pdf.php?key=cGFydGlhbHw5MDE4MngxODY0eDE5fDQxOHw0MjI&f=OTAxODJ4MTg2NHgxOS00MTgtNDIy&one=1.

    Google Scholar 

  112. Van Duyse. Macrostomes congénitaux avec tumeurs préauriculaires et dermoïdes de l’oeil. Ann Société Médecine Gand. 1882. Aout [cited 2020 Apr 2];36. https://archive.org/details/b2163774x

  113. Duyse V. Bride dermoide oculo-palpébrale et colobome partiel de la paupière avec remarques sur la génese de ces anomalies. Ann Ocul. 1882;LXXXXVIII(3 & 4):101–32.

    Google Scholar 

  114. Morian R. Über die schräge Gesichtsspalte (about oblique facial clefts). Arch Klin Chir. 1887;35:245–88.

    Google Scholar 

  115. Laroche V. Essai d’anatomie pathologique sur les monstruosités ou vices de conformation primitifs de la face. [Paris]: thése de medecine,Faculté de Médecine de Paris; 1823.

    Google Scholar 

  116. Grünberg K. Die Gesichtsspalten und die zu ihnen in genetischer Beziehung stehenden anderweitigen Mißbildungen des Gesichts. In: Swalbe E, editor. Die morphologie der missbildüngen des menschen und der tiere [Internet]. Jena: von Gustav Fischer; 1909. p. 113–204. https://archive.org/details/b21506899_0002.

    Google Scholar 

  117. Harkins CS, Berlin A, Harding RL, Longacre JJ, Snodgrasse RM. A classification of cleft lip and cleft palate. Plast Reconstr Surg. 1962;29(1):31–9. http://journals.lww.com/00006534-196201000-00005.

    Article  CAS  Google Scholar 

  118. Sedano HO, Michael Cohen M, Jirasek J, Gorlin RJ. Frontonasal dysplasia. J Pediatr. 1970;76(6):906–13. https://linkinghub.elsevier.com/retrieve/pii/S0022347670803742.

    Article  CAS  PubMed  Google Scholar 

  119. Greig DM. Hypertelorism. A hitherto undifferentiated congenital cranio-facial deformity. Edinb Med J. 1924;XXXI(X):560–93.

    Google Scholar 

  120. Richmond C. Paul Tessier. The Guardian. 2008. https://www.theguardian.com/science/2008/aug/28/medicalresearch.highereducation.

  121. Tessier P. Complete and forme fruste vertical and oblique orbito-facial clefts (colobomas). Ann Chir Plast. 1969;14(4):301–11.

    CAS  PubMed  Google Scholar 

  122. Tessier P. Colobomas: vertical and oblique complete facial clefts. Simultaneous operation of the eyelid, inner canthus, cheek nose and lip Orbitomaxillary bone graft. Panminerva Med. 1969b;11(3):95–101.

    CAS  PubMed  Google Scholar 

  123. Tessier P, Guiot G, Rougerie J, Delbet JP, Pastoriza P. Hypertelorism: cranio-naso-orbito-facial and subethmoid osteotomy. Panminerva Med. 1969;11(3):102–16.

    CAS  PubMed  Google Scholar 

  124. Orbital TP. Hypertelorism: I. Successive surgical attempts. Material and methods. Causes and mechanisms. Scand J Plast Reconstr Surg. 1972;6(2):135–55. https://doi.org/10.3109/02844317209036714.

    Article  Google Scholar 

  125. Tessier P, Guiot G, Derome P. Orbital Hypertelorism: II. Definite treatment of orbital hypertelorism (OR.H.) by craniofacial or by extracranial osteotomies. Scand J Plast Reconstr Surg. 1973;7(1):39–58. https://doi.org/10.3109/02844317309072417.

    Article  CAS  PubMed  Google Scholar 

  126. Tessier P. Orbital hypertelorism. Fortschr Kiefer Gesichtschir. 1974;18:14–27.

    CAS  PubMed  Google Scholar 

  127. Tessier P. Experiences in the treatment of orbital hypertelorism. Plast Reconstr Surg. 1974;53(1):1–18.

    Article  CAS  PubMed  Google Scholar 

  128. Tessier P. Anatomical classification of facial, cranio-facial and latero-facial clefts. J Maxillofac Surg. 1976;4:69–92. https://linkinghub.elsevier.com/retrieve/pii/S0301050376800136.

    Article  CAS  PubMed  Google Scholar 

  129. Nouvelle TP. Classification anatomique des fentes faciales cranio-faciales et latéro-latérales, leur répartition autour de l’orbite. In: Rougier J, Société française d’ophtalmologie, editors. Chirurgie plastique orbito-palpébrale. Paris, New York: Masson; 1977.

    Google Scholar 

  130. Vermeij-Keers C, Mazzola RF, Van der Meulen JC, Strickler M. Cerebro-craniofacial and craniofacial malformations: an embryological analysis. Cleft Palate J. 1983;20(2):128–45.

    CAS  PubMed  Google Scholar 

  131. DeMyer W. Median facial malformations and their implications for brain malformations. Birth Defects Orig Artic Ser. 1975;11(7):155–81.

    CAS  PubMed  Google Scholar 

  132. Whitaker LA, Pashayan H, Reichman J. A proposed new classification of craniofacial anomalies. Cleft Palate J. 1981;18(3):161–76.

    CAS  PubMed  Google Scholar 

  133. van der Meulen JC, Mazzola R, Vermey-Keers C, Strieker M, Raphael B. A morphogenetic classification of craniofacial malformations. Plast Reconstr Surg. 1983;71(4):560–72. http://journals.lww.com/00006534-198304000-00022.

    Article  PubMed  Google Scholar 

  134. Tessier P. Introduction aux dysplasies oto-mandibulaires (D.O.M.) ou “Vingt ans après”. Ann Chir Plast Esthet. 2001;46(5):381–4. https://linkinghub.elsevier.com/retrieve/pii/S029412600100053X.

    Article  CAS  PubMed  Google Scholar 

  135. Tessier P, Ciminello FS, Wolfe SA. The arrhinias. Scand J Plast Reconstr Surg Hand Surg [Internet]. 2009;43(4):177–96. https://doi.org/10.1080/02844310802517259.

    Article  PubMed  Google Scholar 

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Pellerin, P., da Silva Freitas, R. (2023). Mechanisms, Etiology, and Classification of Rare Clefts. In: Alonso, N., Freitas, R.d.S., Tonello, C., Pellerin, P. (eds) Facial Reconstruction of Unusual Facial Clefts. Springer, Cham. https://doi.org/10.1007/978-3-031-40926-4_3

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