Advertisement

Syndromic Eye Anomalies

  • Robert M. VerdijkEmail author
  • Martina C. Herwig-Carl
Chapter
  • 65 Downloads

Abstract

The knowledge of syndromic eye abnormalities is of central importance for the correlation of different combinations of malformations of the eye and other organs in order to determine an exact syndrome diagnosis in spontaneous abortions, pregnancy terminations, and neonates born with multiple congenital malformations. An exact diagnosis not only can provide prognostic information for the index case but also may be helpful in determining the risks for future pregnancies of the same parents. Syndromes may be the result of gross chromosomal abnormalities such as triploidy, trisomy, or monosomy, with a low risk for repeat pregnancy. The detection of monogenic heritable syndromes may offer the possibility of prenatal testing of future offspring. Known malformation sequences of unknown genetic cause also may be characterized by particular ocular anomalies.

Keywords

Syndrome Triploidy Trisomy Germline mutation Developmental malformation Choristoma Patau syndrome Cyclopia Microphthalmia Cryptophthalmia Ciliopathy 

References

  1. 1.
    Toufaily MH, Roberts DJ, Westgate MN, Holmes LB. Triploidy: Variation of phenotype. Am J Clin Pathol. 2016;145:86–95.  https://doi.org/10.1093/ajcp/aqv012.CrossRefPubMedGoogle Scholar
  2. 2.
    Tarkkanen A, Merenmies L, Rapola J. Ocular pathology in triploidy (69-XXY). Ophthalmologica. 1971;163:90–7.  https://doi.org/10.1159/000306327.CrossRefPubMedGoogle Scholar
  3. 3.
    Howard RO, Boué J, Deluchat C, Albert DM, Lahav M. The eyes of embryos with chromosome abnormalities. Am J Ophthalmol. 1974;78:167–88.CrossRefGoogle Scholar
  4. 4.
    Fulton AB, Howard RO, Albert DM, Hsia YE, Packman S. Ocular findings in triploidy. Am J Ophthalmol. 1977;84:859–67.CrossRefGoogle Scholar
  5. 5.
    Wellesley D, Dolk H, Boyd PA, Greenlees R, Haeusler M, Nelen V, et al. Rare chromosome abnormalities, prevalence and prenatal diagnosis rates from population-based congenital anomaly registers in Europe. Eur J Hum Genet. 2012;20:521–6.  https://doi.org/10.1038/ejhg.2011.246.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Boghossian NS, Hansen NI, Bell EF, Stoll BJ, Murray JC, Carey JC, et al. Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Mortality and morbidity of VLBW infants with trisomy 13 or trisomy 18. Pediatrics. 2014;133:226–35.  https://doi.org/10.1542/peds.2013-1702.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Wu J, Springett A, Morris JK. Survival of trisomy 18 (Edwards syndrome) and trisomy 13 (Patau Syndrome) in England and Wales: 2004-2011. Am J Med Genet A. 2013;161A:2512–8.  https://doi.org/10.1002/ajmg.a.36127.CrossRefPubMedGoogle Scholar
  8. 8.
    Scriven PN, Flinter FA, Braude PR, Ogilvie CM. Robertsonian translocations--reproductive risks and indications for preimplantation genetic diagnosis. Hum Reprod. 2001;16:2267–73.  https://doi.org/10.1093/humrep/16.11.2267.CrossRefPubMedGoogle Scholar
  9. 9.
    Veld PA, Weber RF, Los FJ, den Hollander N, Dhont M, Pieters MH, Van Hemel JO. Two cases of Robertsonian translocations in oligozoospermic males and their consequences for pregnancies induced by intracytoplasmic sperm injection. Hum Reprod. 1997;12:1642–4.  https://doi.org/10.1093/humrep/12.8.1642.CrossRefPubMedGoogle Scholar
  10. 10.
    Munné S, Escudero T, Sandalinas M, Sable D, Cohen J. Gamete segregation in female carriers of Robertsonian translocations. Cytogenet Cell Genet. 2000;90:303–8.  https://doi.org/10.1159/000056793.CrossRefPubMedGoogle Scholar
  11. 11.
    Lau TK, Cheung SW, Lo PS, Pursley AN, Chan MK, Jiang F, et al. Non-invasive prenatal testing for fetal chromosomal abnormalities by low-coverage whole-genome sequencing of maternal plasma DNA: review of 1982 consecutive cases in a single center. Ultrasound Obstet Gynecol. 2014;43:254–64.  https://doi.org/10.1002/uog.13277.CrossRefPubMedGoogle Scholar
  12. 12.
    Caba L, Rusu C, Butnariu L, Panzaru M, Braha E, Volosciuc M, et al. Phenotypic variability in Patau syndrome. Rev Med Chir Soc Med Nat Iasi. 2013;117:321–7.PubMedGoogle Scholar
  13. 13.
    Herwig MC, Müller AM, Holz FG, Loeffler KU. Morphologic analysis of artifacts in human fetal eyes confounding histopathologic investigations. Invest Ophthalmol Vis Sci. 2011;52:2712–8.  https://doi.org/10.1167/iovs.10-6301.CrossRefPubMedGoogle Scholar
  14. 14.
    Hoepner J, Yanoff M. Ocular anomalies in trisomy 13-15: an analysis of 13 eyes with two new findings. Am J Ophthalmol. 1972;74:729–37.CrossRefGoogle Scholar
  15. 15.
    Lueder GT. Clinical ocular abnormalities in infants with trisomy 13. Am J Ophthalmol. 2006;141:1057–60.  https://doi.org/10.1016/j.ajo.2005.12.048.CrossRefPubMedGoogle Scholar
  16. 16.
    Koole FD, Velzeboer CM, van der Harten JJ. Ocular abnormalities in Patau syndrome (chromosome 13 trisomy syndrome). Ophthalmic Paediatr Genet. 1990;11:15–21.CrossRefGoogle Scholar
  17. 17.
    Jakobiec FA. Ocular anatomy, embryology, and teratology. Philadelphia: Harper & Row; 1982.Google Scholar
  18. 18.
    Baltensperger A, Haischer G, Rohena L. Rare case of live born with confirmed mosaic trisomy 17 and review of the literature. Clin Case Rep. 2016;4:420–4.  https://doi.org/10.1002/ccr3.397.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Hassold T, Abruzzo M, Adkins K, Griffin D, Merrill M, Millie E, et al. Human aneuploidy: incidence, origin, and etiology. Environ Mol Mutagen. 1996;28:167–75.  https://doi.org/10.1002/(SICI)1098-2280(1996)28:3<167:AID-EM2>3.0.CO;2-B.CrossRefPubMedGoogle Scholar
  20. 20.
    Daber R, Chapman KA, Ruchelli E, Kasperski S, Mulchandani S, Thiel BD, et al. Mosaic trisomy 17: variable clinical and cytogenetic presentation. Am J Med Genet A. 2011;155A:2489–95.CrossRefGoogle Scholar
  21. 21.
    Cierna Z, Janega P, Grochal F, Ferianec V, Braxatorisova T, Strieskova L, et al. The first reported case of Meckel-Gruber Syndrome associated with abnormal karyotype mosaic trisomy 17. Pediatr Dev Pathol. 2017;20:449–54.  https://doi.org/10.1177/1093526616689184.CrossRefPubMedGoogle Scholar
  22. 22.
    Calderone JP, Chess J, Borodic G, Albert DM. Intraocular pathology of trisomy 18 (Edwards’s syndrome): report of a case and review of the literature. Br J Ophthalmol. 1983;67:162–9.  https://doi.org/10.1136/bjo.67.3.162.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Cereda A, Carey JC. The trisomy 18 syndrome. Orphanet J Rare Dis. 2012;7:81.  https://doi.org/10.1186/1750-1172-7-81.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ginsberg J, Perrin EV, Sueoka WT. Ocular manifestations of trisomy 18. Am J Ophthalmol. 1968;66:59–67.CrossRefGoogle Scholar
  25. 25.
    Pe’er J, Braun JT. Ocular pathology in trisomy 18 (Edwards’ syndrome). Ophthalmologica. 1986;192:176–8.  https://doi.org/10.1159/000309637.CrossRefPubMedGoogle Scholar
  26. 26.
    Mullaney J. Ocular pathology in trisomy 18 (Edwards’ syndrome). Am J Ophthalmol. 1973;76:246–54.CrossRefGoogle Scholar
  27. 27.
    Mirmohammadsadeghi A, Akbari MR, Malekpoor A. Ocular manifestations in Edward’s syndrome, a case report and literature review. J Curr Ophthalmol. 2017;29:329–31.  https://doi.org/10.1016/j.joco.2017.06.005.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    de Graaf G, Engelen JJM, Gijsbers ACJ, Hochstenbach R, Hoffer MJV, Kooper AJA, et al. Estimates of live birth prevalence of children with Down syndrome in the period 1991-2015 in the Netherlands. J Intellect Disabil Res. 2017;61:461–70.  https://doi.org/10.1111/jir.12371.CrossRefPubMedGoogle Scholar
  29. 29.
    Müller PL, Löffler KU, Kohlhaas M, Holz FG, Herwig-Carl MC. Morphologische Hornhautveränderungen nach Crosslinking bei Keratokonus (Morphologic Corneal Changes after Crosslinking for Keratoconus). Klin Monbl Augenheilkd. 2018;235:809–19.  https://doi.org/10.1055/s-0043-102577.CrossRefPubMedGoogle Scholar
  30. 30.
    Haargaard B, Wohlfahrt J, Fledelius HC, Rosenberg T, Melbye M. A nationwide Danish study of 1027 cases of congenital/infantile cataracts: etiological and clinical classifications. Ophthalmology. 2004;111:2292–8.  https://doi.org/10.1016/j.ophtha.2004.06.024.CrossRefPubMedGoogle Scholar
  31. 31.
    Brooke Williams RD. Brushfield spots and Wolfflin nodules in the iris: an appraisal in handicapped children. Dev Med Child Neurol. 1981;23:646–9.CrossRefGoogle Scholar
  32. 32.
    Berk AT, Saatci AO, Erçal MD, Tunç M, Ergin M. Ocular findings in 55 patients with Down’s syndrome. Ophthalmic Genet. 1996;17:15–9.CrossRefGoogle Scholar
  33. 33.
    O’Brien S, Wang J, Smith HA, Donaldson DL, Haider KM, Roberts GJ, et al. Macular structural characteristics in children with Down syndrome. Graefes Arch Clin Exp Ophthalmol. 2015;253:2317–23.  https://doi.org/10.1007/s00417-015-3088-x.CrossRefPubMedGoogle Scholar
  34. 34.
    Gravholt CH, Stochholm K. The epidemiology of Turner syndrome. Int Congr Ser. 2006;1298:139–45.  https://doi.org/10.1016/j.ics.2006.06.009.CrossRefGoogle Scholar
  35. 35.
    Chrousos GA, Ross JL, Chrousos G, Chu FC, Kenigsberg D, Cutler G Jr, Loriaux DL. Ocular findings in Turner syndrome. A prospective study. Ophthalmology. 1984;91:926–8.CrossRefGoogle Scholar
  36. 36.
    Adhikary HP. Ocular manifestations of Turner’s syndrome. Trans Ophthalmol Soc U K. 1981;101:395–6.PubMedGoogle Scholar
  37. 37.
    Wikiera B, Mulak M, Koltowska-Haggstrom M, Noczynska A. The presence of eye defects in patients with Turner syndrome is irrespective of their karyotype. Clin Endocrinol (Oxf). 2015;83:842–8.  https://doi.org/10.1111/cen.12794.CrossRefGoogle Scholar
  38. 38.
    Strungaru MH, Mah D, Chan CC. Focal limbal stem cell deficiency in Turner syndrome: report of two patients and review of the literature. Cornea. 2014;33:207–9.  https://doi.org/10.1097/ICO.0000000000000040.CrossRefPubMedGoogle Scholar
  39. 39.
    Macsai M, Maguen E, Nucci P. Keratoconus and Turner’s syndrome. Cornea. 1997;16:534–6.PubMedGoogle Scholar
  40. 40.
    Fallet-Bianco C. Neuropathology of holoprosencephaly. Am J Med Genet C Semin Med Genet. 2018;178:214–28.  https://doi.org/10.1002/ajmg.c.31623.CrossRefPubMedGoogle Scholar
  41. 41.
    Fitz CR. Holoprosencephaly and related entities. Neuroradiology. 1983;25:225–38.CrossRefGoogle Scholar
  42. 42.
    Giger FA, Houart C. The birth of the eye vesicle: when fate decision equals morphogenesis. Front Neurosci. 2018;12:87.  https://doi.org/10.3389/fnins.2018.00087.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Fryns JP, Legius E, Moerman P, Vandenberghe K, Van den Berghe H. Apparently new “anophthalmia-plus” syndrome in sibs. Am J Med Genet. 1995;58:113–4.  https://doi.org/10.1002/ajmg.1320580204.CrossRefPubMedGoogle Scholar
  44. 44.
    Warburg M, Jensen H, Prause JU, Bolund S, Skovby F, Miranda MJ. Anophthalmia-microphthalmia-oblique clefting syndrome: confirmation of the Fryns anophthalmia syndrome. Am J Med Genet. 1997;73:36–40.CrossRefGoogle Scholar
  45. 45.
    Wiltshire E, Moore M, Casey T, Smith G, Smith S, Thompson E. Fryns “Anophthalmia-Plus” syndrome associated with developmental regression. Clin Dysmorphol. 2003;12:41–3.  https://doi.org/10.1097/01.mcd.0000049263.13501.37.CrossRefPubMedGoogle Scholar
  46. 46.
    Jayasinghe C, Gembruch U, Kuchelmeister K, Körber F, Müller AM. Fryns anophthalmia-plus syndrome in an 18-week-old fetus. Pediatr Dev Pathol. 2012;15:58–61.  https://doi.org/10.2350/10-07-0880-CR.1.CrossRefPubMedGoogle Scholar
  47. 47.
    Fryns JP, Moerman F, Goddeeris P, Bossuyt C, Van den Berghe H. A new lethal syndrome with cloudy corneae, diaphragmatic defects and distal limb deformities. Hum Genet. 1979;50:65–70.CrossRefGoogle Scholar
  48. 48.
    Pierson DM, Taboada E, Butler MG. Eye abnormalities in Fryns syndrome. Am J Med Genet A. 2004;125A:273–7.  https://doi.org/10.1002/ajmg.a.20520.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Cursiefen C, Schlötzer-Schrehardt U, Holbach LM, Vieth M, Kuchelmeister K, Stolte M. Ocular findings in Fryns syndrome. Acta Ophthalmol Scand. 2000;78:710–3.CrossRefGoogle Scholar
  50. 50.
    Aymé S, Julian C, Gambarelli D, Mariotti B, Luciani A, Sudan N, et al. Fryns syndrome: report on 8 new cases. Clin Genet. 1989;35:191–201.CrossRefGoogle Scholar
  51. 51.
    Lenz W. Recessiv-geschlechtsgebundene Mikrophthalmie mit multiplen Missbildungen (Recessive, sex-limited microphthalmia with multiple abnormalities). Z Kinderheilkd. 1955;77:384–90.CrossRefGoogle Scholar
  52. 52.
    Ng D. Lenz microphthalmia syndrome. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Stephens K, Amemiya A, editors. GeneReviews® [Internet]. Seattle (WA): University of Washington; 2002. [updated 2014]. http://www.ncbi.nlm.nih.gov/books/NBK1521/.Google Scholar
  53. 53.
    Ng D, Thakker N, Corcoran CM, Donnai D, Perveen R, Schneider A, et al. Oculofaciocardiodental and Lenz microphthalmia syndromes result from distinct classes of mutations in BCOR. Nat Genet. 2004;36:411–6.  https://doi.org/10.1038/ng1321.CrossRefPubMedGoogle Scholar
  54. 54.
    Suzumori N, Kaname T, Muramatsu Y, Yanagi K, Kumagai K, Mizuno S, et al. Prenatal diagnosis of X-linked recessive Lenz microphthalmia syndrome. J Obstet Gynaecol Res. 2013;39:1545–7.  https://doi.org/10.1111/jog.12081.CrossRefPubMedGoogle Scholar
  55. 55.
    Esmailpour T, Riazifar H, Liu L, Donkervoort S, Huang VH, Madaan S, et al. A splice donor mutation in NAA10 results in the dysregulation of the retinoic acid signalling pathway and causes Lenz microphthalmia syndrome. J Med Genet. 2014;51:185–96.  https://doi.org/10.1136/jmedgenet-2013-101660.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Ng D, Hadley DW, Tifft CJ, Biesecker LG. Genetic heterogeneity of syndromic X-linked recessive microphthalmia-anophthalmia: is Lenz microphthalmia a single disorder? Am J Med Genet. 2002;110:308–14.  https://doi.org/10.1002/ajmg.10484.CrossRefPubMedGoogle Scholar
  57. 57.
    Al-Gazali LI, Mueller RF, Caine A, Antoniou A, McCartney A, Fitchett M, Dennis NR. Two 46,XX,t(X;Y) females with linear skin defects and congenital microphthalmia: a new syndrome at Xp22.3. J Med Genet. 1990;27:59–63.  https://doi.org/10.1136/jmg.27.1.59.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Cain CC, Saul D, Attanasio L, Oehler E, Hamosh A, Blakemore K, Stetten G. Microphthalmia with linear skin defects (MLS) syndrome evaluated by prenatal karyotyping, FISH and array comparative genomic hybridization. Prenat Diagn. 2007;27:373–9.  https://doi.org/10.1002/pd.1674.CrossRefPubMedGoogle Scholar
  59. 59.
    Cape CJ, Zaidman GW, Beck AD, Kaufman AH. Phenotypic variation in ophthalmic manifestations of MIDAS syndrome (microphthalmia, dermal aplasia, and sclerocornea). Arch Ophthalmol. 2004;122:1070–4.  https://doi.org/10.1001/archopht.122.7.1070.CrossRefPubMedGoogle Scholar
  60. 60.
    Carman KB, Yakut A, Sabuncu I, Yarar C. MIDAS (microphthalmia, dermal aplasia, sclerocornea) syndrome with central nervous system abnormalities. Clin Dysmorphol. 2009;18:234–5.  https://doi.org/10.1097/MCD.0b013e32832e38a6.CrossRefPubMedGoogle Scholar
  61. 61.
    Herwig MC, Loeffler KU, Gembruch U, Kuchelmeister K, Müller AM. Anterior segment developmental anomalies in a 33-week-old fetus with MIDAS syndrome. Pediatr Dev Pathol. 2014;17:491–5.  https://doi.org/10.2350/13-11-1408-CR.1.CrossRefPubMedGoogle Scholar
  62. 62.
    Happle R, Daniëls O, Koopman RJ. MIDAS syndrome (microphthalmia, dermal aplasia, and sclerocornea): an X-linked phenotype distinct from Goltz syndrome. Am J Med Genet. 1993;47:710–3.  https://doi.org/10.1002/ajmg.1320470525.CrossRefPubMedGoogle Scholar
  63. 63.
    Kapur R, Tu EY, Toyran S, Shah P, Vangveeravong S, Lloyd WC 3rd, Edward DP. Corneal pathology in microphthalmia with linear skin defects syndrome. Cornea. 2008;27:734–8.  https://doi.org/10.1097/QAI.0b013e31815b834d.CrossRefPubMedGoogle Scholar
  64. 64.
    Naumann GOH. Pathologie des Auges. In: Spezielle pathologische Anatomie. Berlin, Heidelberg: Springer; 1980.  https://doi.org/10.1007/978-3-642-96500-5.
  65. 65.
    Barisic I, Odak L, Loane M, Garne E, Wellesley D, Calzolari E, et al. Fraser syndrome: epidemiological study in a European population. Am J Med Genet A. 2013;161A:1012–8.  https://doi.org/10.1002/ajmg.a.35839.CrossRefPubMedGoogle Scholar
  66. 66.
    Slavotinek AM, Tifft CJ. Fraser syndrome and cryptophthalmos: review of the diagnostic criteria and evidence for phenotypic modules in complex malformation syndromes. J Med Genet. 2002;39:623–33.  https://doi.org/10.1136/jmg.39.9.623.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    van Haelst MM, Scambler PJ, Hennekam RCM. Fraser syndrome: a clinical study of 59 cases and evaluation of diagnostic criteria. Am J Med Genet A. 2007;143A:3194–203.  https://doi.org/10.1002/ajmg.a.31951.CrossRefPubMedGoogle Scholar
  68. 68.
    Thomas IT, Frias JL, Felix V, Sanchez de Leon L, Hernandez RA, Jones MC. Isolated and syndromic cryptophthalmos. Am J Med Genet. 1986;25:85–98.  https://doi.org/10.1002/ajmg.1320250111.CrossRefPubMedGoogle Scholar
  69. 69.
    Vogel MJ, van Zon P, Brueton L, Gijzen M, van Tuil MC, Cox P, et al. Mutations in GRIP1 cause Fraser syndrome. J Med Genet. 2012;49:303–6.  https://doi.org/10.1136/jmedgenet-2011-100590.CrossRefPubMedGoogle Scholar
  70. 70.
    Goldenhar M. Associations malformatives de l’oeil et de l’oreille, en particulier le syndrome dermoide epibulbaue — appendices auriculaires — fistula auris congenita et ses relations avec la dysostose mandibulo-faciale. J Genet Hum. 1952;1:243–82.Google Scholar
  71. 71.
    Bogusiak K, Puch A, Arkuszewski P. Goldenhar syndrome: current perspectives. World J Pediatr. 2017;13:405–15.  https://doi.org/10.1007/s12519-017-0048-z.CrossRefPubMedGoogle Scholar
  72. 72.
    Herwig MC, Gembruch U, Born M, Gevensleben H, Loeffler KU, Müller AM. Preterm diagnosis of choristoma and choroidal coloboma in Goldenhar’s syndrome. Pediatr Dev Pathol. 2011;14:322–6.  https://doi.org/10.2350/10-07-0874-CR.1.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Mansour AM, Wang F, Henkind P, Goldberg R, Shprintzen R. Ocular findings in the facioauriculovertebral sequence (Goldenhar-Gorlin syndrome). Am J Ophthalmol. 1985;100:555–9.CrossRefGoogle Scholar
  74. 74.
    Sharma D, Murki S, Pratap T, Vasikarla M. Cat eye syndrome. BMJ Case Rep. 2014;2014:bcr2014203923.  https://doi.org/10.1136/bcr-2014-203923.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Kunze J. Wiedemanns Atlas klinischer Syndrome: Phänomenologie - Ätiologie – Differenzialdiagnose. Stuttgart: Schattauer; 2010.Google Scholar
  76. 76.
    Rosias PR, Sijstermans JM, Theunissen PM, Pulles-Heintzberger CF, De Die-Smulders CE, Engelen JJ, Van Der Meer SB. Phenotypic variability of the cat eye syndrome. Case report and review of the literature. Genet Couns. 2001;12:273–82.PubMedGoogle Scholar
  77. 77.
    Berends MJ, Tan-Sindhunata G, Leegte B, van Essen AJ. Phenotypic variability of cat-eye syndrome. Genet Couns. 2001;12:23–34.PubMedGoogle Scholar
  78. 78.
    Shaheen R, Szymanska K, Basu B, Patel N, Ewida N, Faqeih E, et al. Characterizing the morbid genome of ciliopathies. Genome Biol. 2016;17:242.  https://doi.org/10.1186/s13059-016-1099-5.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Hartill V, Szymanska K, Sharif SM, Wheway G, Johnson CA. Meckel-Gruber syndrome: an update on diagnosis, clinical management, and research advances. Front Pediatr. 2017;5:244.  https://doi.org/10.3389/fped.2017.00244.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Parisi MA. Clinical and molecular features of Joubert syndrome and related disorders. Am J Med Genet C Semin Med Genet. 2009;151C:326–40.  https://doi.org/10.1002/ajmg.c.30229.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    MacRae DW, Howard RO, Albert DM, Hsia YE. Ocular manifestations of the Meckel syndrome. Arch Ophthalmol. 1972;88:106–13.CrossRefGoogle Scholar
  82. 82.
    Sturm V, Leiba H, Menke MN, Valente EM, Poretti A, Landau K, Boltshauser E. Ophthalmological findings in Joubert syndrome. Eye (Lond). 2010;24:222–5.  https://doi.org/10.1038/eye.2009.116.CrossRefGoogle Scholar
  83. 83.
    Vajsar J, Schachter H. Walker-Warburg syndrome. Orphanet J Rare Dis. 2006;1:29.  https://doi.org/10.1186/1750-1172-1-29.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Crowe C, Jassani M, Dickerman L. The prenatal diagnosis of the Walker-Warburg syndrome. Prenat Diagn. 1986;6:177–85.CrossRefGoogle Scholar
  85. 85.
    Farrell SA, Toi A, Leadman ML, Davidson RG, Caco C. Prenatal diagnosis of retinal detachment in Walker-Warburg syndrome. Am J Med Genet. 1987;28:619–24.  https://doi.org/10.1002/ajmg.1320280309.CrossRefPubMedGoogle Scholar
  86. 86.
    Gasser B, Lindner V, Dreyfus M, Feidt X, Leissner P, Treisser A, Stoll C. Prenatal diagnosis of Walker-Warburg syndrome in three sibs. Am J Med Genet. 1998;76:107–10.CrossRefGoogle Scholar
  87. 87.
    Sanders DG, Mooy CM. Ocular findings in cerebro-ocular-myopathy syndrome (COMS). A possible role of growth factors? Int Ophthalmol. 1993;17:223–8.CrossRefGoogle Scholar
  88. 88.
    de Jong JG, Delleman JW, Houben M, Manschot WA, de Minjer A, Mol J, Slooff JL. Agenesis of the corpus callosum, infantile spasms, ocular anomalies (Aicardi’s syndrome). Clinical and pathologic findings. Neurology. 1976;26:1152–8.  https://doi.org/10.1212/wnl.26.12.1152.CrossRefPubMedGoogle Scholar
  89. 89.
    Aicardi J. Aicardi syndrome. Brain Dev. 2005;27:164–71.  https://doi.org/10.1016/j.braindev.2003.11.011.CrossRefPubMedGoogle Scholar
  90. 90.
    Trifiletti RR, Incorpora G, Polizzi A, Cocuzza MD, Bolan EA, Parano E. Aicardi syndrome with multiple tumors: a case report with literature review. Brain Dev. 1995;17:283–5.CrossRefGoogle Scholar
  91. 91.
    Wharton JD, Johnson S, Connelly JA, Hills T, Gingles L, Wood M, et al. High-dose chemotherapy is efficacious and well tolerated in a toddler with Aicardi syndrome and malignant sacrococcygeal teratoma. J Pediatr Hematol Oncol. 2018;40:e467–9.  https://doi.org/10.1097/MPH.0000000000001091.CrossRefPubMedGoogle Scholar
  92. 92.
    Hsu P, Ma A, Wilson M, Williams G, Curotta J, Munns CF, Mehr S. CHARGE syndrome: a review. J Paediatr Child Health. 2014;50:504–11.  https://doi.org/10.1111/jpc.12497.CrossRefPubMedGoogle Scholar
  93. 93.
    Fledelius HC. Ultrasonic evaluation of microphthalmos and coloboma. A discussion of 3 cases, with emphasis on microphthalmos with orbital cyst. Acta Ophthalmol Scand Suppl. 1996;219:23–6.Google Scholar
  94. 94.
    de Krijger RR, Mooy CM, van Hemel JO, Sulkers EJ, Kros JM, Bartelings MM and Govaerts LCP. CHARGE association-related ocular pathology in a newborn with partial trisomy 19q and partial monosomy 21q, from a maternal translocation (19;21) (q13.1;q22.3). Pediatr Dev Pathol. 1999;2:577–81.  https://doi.org/10.1007/s100249900165.CrossRefGoogle Scholar
  95. 95.
    Hale CL, Niederriter AN, Green GE, Martin DM. Atypical phenotypes associated with pathogenic CHD7 variants and a proposal for broadening CHARGE syndrome clinical diagnostic criteria. Am J Med Genet A. 2016;170A:344–54.  https://doi.org/10.1002/ajmg.a.37435.CrossRefPubMedGoogle Scholar
  96. 96.
    Glueckert R, Rask-Andersen H, Sergi C, Schmutzhard J, Mueller B, Beckmann F, et al. Histology and synchrotron radiation-based microtomography of the inner ear in a molecularly confirmed case of CHARGE syndrome. Am J Med Genet A. 2010;152A:665–73.  https://doi.org/10.1002/ajmg.a.33321.CrossRefPubMedGoogle Scholar
  97. 97.
    Blake KD, Prasad C. CHARGE syndrome. Orphanet J Rare Dis. 2006;1:34.  https://doi.org/10.1186/1750-1172-1-34.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Zentner GE, Layman WS, Martin DM, Scacheri PC. Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A. 2010;152A:674–86.  https://doi.org/10.1002/ajmg.a.33323.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Hayashi N, Valdes-Dapena M, Green WR. CHARGE association: histopathological report of two cases and a review. J Pediatr Ophthalmol Strabismus. 1998;35:100–6.PubMedGoogle Scholar
  100. 100.
    Hittner HM, Hirsch NJ, Kreh GM, Rudolph AJ. Colobomatous microphthalmia, heart disease, hearing loss, and mental retardation--a syndrome. J Pediatr Ophthalmol Strabismus. 1979;16:122–8.PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Pathology, Section Ophthalmic PathologyErasmus MC University Medical Center RotterdamRotterdamThe Netherlands
  2. 2.Department of PathologyLeiden University Medical CenterLeidenThe Netherlands
  3. 3.Department of OphthalmologyUniversity Hospital BonnBonnGermany

Personalised recommendations