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420
Figure 14–20. Hyaloid artery bifurcation associated with fetal cataract
detection in utero.
Chapter 14 The Fetal Eye
are formed because of mucus accumulation. Complete
obstruction may lead to an increased respiratory effort or
even respiratory distress. In such cases, probing of the duct
or silicone intubation is indicated.
89 , 90 , 92
Although congenital dacryocystoceles may resolve
without surgical intervention, some become infected and
require systemic antibiotic treatment and even surgical
drainage.
gested if a cystic mass is visualized adjacent to the orbit and
the base of the nose.
88
Prenatal sonographic diagnosis should be sug-
89 – 96
The differential diagnosis includes
other anomalies in this region, such as encephalocele or
hemangioma. Bilateral dacrocystocele has been detected in
utero ( Figure 14–26 ). Other periorbital findings are an epidermoid cyst that was detected in our patient at 29 weeks’
gestation ( Figure 14–27 ) and retinal coloboma diagnosed
prenatally by Bault and Quarello
97
( Figure 14–28 ).
A
B
TRAUMA OF THE EYE
DURING AMNIOCENTESIS
The possible association between amniocentesis and fetal
damage is well known. However, there are only a few
cases reported on ophthalmologic complications;
98 – 103
in
these case reports, cystic lesions, perforations, and scars
were noted in the different parts of the eye. In some of the
reports, the damage was corrected by surgery; but in others, the damage was severe, leading to hemianopia, gaze
101
microphthalmia, and total blindness.
palsy,
99
Ultrasound-guided amniocentesis has now become
the standard of care. It is expected that this technique will
reduce to a minimum the incidence of fetal trauma during
the procedure.
PHYSIOLOGIC ASPECTS OF THE FETAL EYE
Fetal Eye Movements
Fetal eye movements are best evaluated by ultrasonographic observation of positional changes of the lenses.
The pattern of fetal eye movements was studied and correlated with the emergence of fetal behavior states.
C
Figure 14–21. Persistent hyaloid vessels (A) Persistent hyperplastic pri-
mary vitreous (PHPV) at 34 postmenstrual weeks in a fetus with trisomy
13. The hyaloid aretery (HA) is fibrotic, going from the retina to the opaque
lens, the ocular globe is small, and the lens is horizontal. (B) A normal eye
with sonolucent lens, and no hyaloid artery visualized at 34 postmenstrual
weeks. (C) Histology of the fetal eye demonstrating the persistent hyaloid
vessels defining the PHPV. (Courtesy of Dr Y. Ben-Arieh.)
Chapter 14 The Fetal Eye
421
A
Figure 14–22. The problematic diagnosis of PHPV before 32 weeks is demonstrated by the following cases. (A) At 15 postmenopausal weeks, the
hyaloid vessels are congested and hyperplastic in a fetus with trisomy 18, which is associated with PHPV. (B) The congested hyaloid vessels form a concentric double halo around the fetal lens at 15 postmenstrual weeks. This anomaly disappeared by 32 weeks, and the pregnancy generated a completely
normal neonate.
Birnholz
104
described four types of eye movements:
1. Type I: single transient linear deviation, usually from
midposition to a lower, outer orbital margin, followed
by a slightly slower return to the initial position
2. Type II: prolonged but single deviation to a medial or
lateral position
B
3. Type III: complex sequence of deviations, including
rotatory components without apparent spatial or
temporal periodicity (these movements are typically
brisk and jerky)
4. Type IV: repetitive or nystagmoid deviations
Birnholz regarded types I and II as slow eye movements, and types III and IV as rapid eye movements.
Arduini and coworkers
105
considered as rapid eye movements rapid nystagmus-like movements with a frequency
>6/min. Eye movements with a frequency <6/min were
defined as slow eye movements.
105
Figure 14–23. Hypotelorism. The orbits ( arrows ) of this fetus at 15
postmenstrual weeks are very close to each other.
Figure 14–24. Retinal detachment diagnosis in a fetus at 26 postmen-
strual weeks. (From Blin G, et al,
77
with permission.)
422
A
Chapter 14 The Fetal Eye
A
B
B
Figure 14–25. A case of ocular rhabdomyosarcoma at 35 postmenstrual
weeks. Transverse section through the fetal skull showing an enlarged left
ocular bulb protruding out of the orbit (A) and after delivery (B) in the
neonate. (Courtesy of Bajram H. Syla. Reproduced, with permission, from
www.thefetus.net.)
C
Figure 14–27.
weeks by two-dimentional US ( A ), three-dimentional US (B), and after
delivery, in the neonate ( C ).
A case of epidermoid cyst detected at 29 postmenstrual
Figure 14–26. A case of bilateral dacrocystocele detected in utero at
30 postmenstrual weeks. (Courtesy of Yinon Gilboa. Reproduced, with
permission, from www.thefetus.net.)
Figure 14–28. A case of fetal retinal coloboma ( arrow ) detected at
16 weeks.
Chapter 14 The Fetal Eye
423
Horimoto and associates
106
noted two types of eye
movements. Those with duration of 0.07 up to 0.6 to
0.8 second were regarded as rapid eye movements. The
others with duration of 0.6 to 0.8 up to 4 to 5 seconds
were considered slow eye movements.
gestational age distribution of the various types of eye
movements have been observed. Birnholz
106
Differences in
104
reported that
type I movements were apparent between 16 and 26 postmenstrual weeks’ gestation, whereas type IV movements
were recognized only after 32 postmenstrual weeks.
The patterns of eye movements, as well as the periodicity of absent eye movements, are important in the
definition of fetal behavioral states. Nijuis and collabora-
107
defined four types of fetal behavior at 36 to 40 post-
tors
menstrual weeks. According to their classification, there
is absence of fetal eye movements in state 1F. In the other
three states, 2F, 3F, and 4F, both slow and rapid eye movements are continually present.
Arduini’s group
105
reported that during quiet phases of
107
fetal behavior, slow eye movements, as well as absence of
eye movement, was recorded. Rapid eye movements were
never observed at this phase of fetal activity. On the other
hand, during the active phases of fetal activity, both slow and
rapid eye movements, as well as the absence of eye movement, could be noted. However, after 36 postmenstrual
weeks, a significant prevalence of rapid eye movements
during the active phases and absence of eye movement
during the quiet phases were observed.
105
A change in fetal eye movements (blinking response)
may be induced by vibroacoustic stimulation. This is part
of the startle response and change in fetal behavior state
occurring in healthy fetuses following stimulation.
Horimoto and colleagues
109
evaluated changes in
107
pupillary diameters in relation to fetal eye movements.
Pupillary diameters were found to be differentiated with
statistical significance into two groups: 9.7% for the
dilated pupil (range 2.1–3.4 mm) and 90.3% for the constricted pupil (range 1.4–1.9 mm). The percentage of
dilated pupils during eye movement period (14.3%) was
significantly greater than that during no eye movement
period (2.3%).
109
This relation between papillary diameter
and eye movement is in agreement with data from adults.
COLOBOMA
Congenital optic coloboma represents an important cause
of childhood visual impairment and blindness; it can be
either isolated or, more often, associated with several
syndromes. Coloboma is a rare malformation consisting
of a wedge malformation in the ocular bulb. Although not
included in any screening protocol, it may be prenatally
diagnosed, at least in some cases, by US ( Figure 14–28 ).
Retinal coloboma can be diagnosed in utero using a
new technique, the so-called virtual fetal eyeground.
However, in our experience the traditional B mode is also
accurate for the detection of coloboma. We also believe
that in cases where a satisfactory sonographic evaluation
of the fetal eyes is possible and accessible, high-resolution
US may be more accurate and informative than magnetic
resonance imaging.
110
97
REFERENCES
1. Robinson GC, Jan JE, Kinnis C. Congenital ocular blindness in children, 1945 to 1984. Am J Dis Child. 1987;141:1321–1324.
2. Goggin M, O’Keefe M. Childhood blindness in the Republic of
Ireland: A national survey. Br J Opthalmol. 1991;75:425–429.
3. Foster A. Gilbert C. Epidemiology of childhood blindness. Eye.
1992;6:173–176.
4. Stoll C, Alembik Y, Dott B, Roth MP. Epidemiology of congenial eye
malformations in 131,760 consecutive births. Opthalmic Pediatr
Genet. 1992;13:179–186.
5. Jay B. Causes of blindness in school children. Br Med J. 1987;294:
1183–1184.
6. Phillips CI, Levy AM, Newton M, Stokoe NL. Blindness in school
children: Importance of heredity, congenial cataract and prematurity. Br J Opthalmol. 1987;71:578–584.
7. Stoll C, Alembik Y, Dott B, Roth MP. Congenital eye malformations
in 212,479 consecutive births. Ann Genet. 1997;40:122–128.
8. Nicolaides KH, Salversen DR, Sijders RJM, Gosdes CM. Fetal facial
defects: Associated malformations and chromosomal abnormalities.
Fetal Diagn Ther. 1993;8:1–9.
9. Wilkie AOM, Amberger JS, McKusick VA. The gene map of congenital malformations. J Med Genet. 1994;31:507–517.
10. Sadler TW, ed. Eye. In: Langsman’s Medical Embryology. 6th ed.
Baltimore: Williams & Wilkins; 1990:338–346.
11. Larsen WJ, ed. Development of the eyes. In: Human Embryology.
4th ed. Churchill Livingstone; Philadelphia. 2001:379–389.
12. Ko M-K, Chi JG, Chang B-L. Hyaloid vascular pattern in the human
fetus. J Pediatr Opthalmol Strabismus. 1985;22:188–193.
13. Birnholz JC, Farrell EE. Fetal hyaloid artery: Timing of regression
with US. Radiology. 1988;166:781–783.
14. Harayama K, Amemiya T, Nishimura H. Development of the eyeball
during fetal life. J Pediatr Ophthalmol Strabismus. 1981;18:37–40.
15. Denis D, Righini M, Scheiner C, et al. Ocular growth in the fetus: 1.
Comparative study of axial length and biometric parameters in the
fetus. Ophthalmologica. 1993;207:117–124.
16. Birnholz JC. Ultrasonic fetal ophthalmology. Early Hum Dev.
1985;12:199–209.
17. de Elejalde MM, Elejalde BR. Ultrasonographic visualization of the
fetal eye. J Craniofac Genet Dev Biol. 1985;5:319–326.
18. Jeanty P, Dramaix-Wilmet M, Van Gansbeke D, Van Regemorter
N, Rodesch F, Fetal ocular biometry by ultrasound. Radiology.
1982;143:513–516.
19. Mayden KL, Tortora M, Berkowitz RL, Bracken M, Hobbins JC.
Orbital diameters: A new parameter for prenatal diagnosis and dating. Am J Obstet Gynecol. 1982;144:289–297.
20. Goldstein I, Tamir A, Zimmer EZ, Itskovitz-Eldor J. Growth of
the fetal orbit and lens in normal pregnancies. Ultrasound Obstet
Gynecol. 1998;12:175–179.
21. Dilmen G, Köktener A, Turhan NO, Tez S. Growth of the fetal lens
and orbit. Int J Gynaecol Obstet. 2002;76(3):267–271.
22. Sukonpan K, Phupong V. Fetal ocular distance in normal pregnancies. J Med Assoc Thai. 2008;91:1318–1322.
23. Achiron R, Gottlieb Z, Yaron Y, et al. The development of the fetal
eye: In utero ultrasonographic measurements of the vitreous and
lens. Prenat Diagn. 1995;15:155–160.
24. Achiron R, Kreiser D, Achiron A. Axial growth of the fetal eye and
evaluation of the hyaloid artery: In utero ultrasonographic study.
Prenat Diagn. 2000;20:894–899.
25. Nelson LB. Diagnosis and management of cataracts in infancy and
childhood. Ophthalmic Surg. 1984;15:688–697.
26. Kohn BA. The differential diagnosis of cataracts in infancy and
childhood. Am J Dis Child. 1976;130:184–192.
27. Merin S, Crawford JS. The etiology of congenital cataracts: a survey
of 386 cases. Can J Ophthalmol. 1971;6:178–182.
28. Taylor D. Congenital cataract: The history, the nature and the practice. Eye. 1998;12:9–36.
29. Walton DS. Eye evaluation in the newborn. In: Oski FA, DeAngelis
CD, Feigin RD, Warshaw JB, eds. Principles and Practice of Pediatrics.
Philadelphia: Lippincott Williams & Wilkins’ 1990:468–470.
30. Shapiro I, Borochowitz Z, Degani S, Dar H, Ibschitz I, Sharf M.
Neu-Laxova syndrome: Prenatal ultrasonographic diagnosis, clinical
and pathological studies and new manifestations. Am J Med Genet.
1992;43:602–605.
424
Chapter 14 The Fetal Eye
31. Zimmer EZ, Bronshtein M, Ophir E, et al. Sonographic diagnosis of
fetal congenital cataracts. Prenat Diagn. 1993;13:503–511.
32. Gaary EA, Rawnsley E, Marin-Padilla JM, Morse CL, Crow HC.
In utero detection of fetal cataracts. J Ultrasound Med. 1993;12:
234–236.
33. Monteagudo A, Timor-Tritsch IE, Friedman AH, Santos R.
Autosomal dominant cataracts of the fetus: Early detection by transvaginal ultrasound. Ultrasound Obstet Gynecol. 1996;8:104–108.
34. Drysdale K, Kyle PM, Sepulveda W. Prenatal detection of congenital
inherited cataracts. Ultrasound Obstet Gynecol. 1997;9:62–63.
35. Romain M, Awoust J, Dugauquier C, van Maldergem L. Prenatal
ultrasound detection of congenital cataract in trisomy 21. Prenat
Diagn. 1999;19:780–782.
36. Pedreira DAL, Diniz EMA, Schultz R, Faro LB, Zugaib M. Fetal
cataract in congenital toxoplasmosis. Ultrasound Obstet Gynecol.
1999;13:266–267.
37. Müllner-Eidenböck A, Amon M, Moser E, Klebermass N.
Persistent fetal vasculature and minimal fetal vascular remnants:
A frequent cause of unilateral congenital cataracts. Ophthalmology.
2004;111:906–913.
38. Zeiter HJ. Congenital microphthalmus. Am J Ophthalmol.
1963;55:910–922.
39. Duke-Elder S, Cooke C. Microphthalmos: Congenital deformities.
In: Duke-Elder S, ed. System of Ophthalmology. Vol 3. St. Louis, MO:
CV Mosby; 1964:488–495.
40. Warburg M. Genetics of microphthalmos. Int Ophthalmol.
1981;4:45–65.
41. Sutcliffe AG, Jones RB, Woodruff G. Eye malformations associated
with treatment with carbamazepine during pregnancy. Ophthalmic
Genet. 1998;19:59–62.
42. Schauer GM, Dunn LK, Godmilow L, Eagle RC, Knisely AS. Prenatal
diagnosis of Fraser syndrome at 18.5 weeks gestation, with autopsy
finding at 19 weeks. Am J Med Genet. 1990;37:583–591.
43. Bronshtein M, Zimmer EZ, Gershoni-Baruch R, Yoffe N, Meyer H,
Blumenfeld Z. First and second trimester diagnosis of fetal ocular
defects and associated anomalies: Report of eight cases. Obstet
Gynecol. 1991;77:443–449.
44. Porges Y, Gershoni-Baruch R, Leibu R, et al. Hereditary microphthalmia with colobomatous cyst. Am J Ophthalmol. 1992;114:30–34.
45. Blazer S, Zimmer EZ, Mezer E, Bronshtein M. Early and late onset
fetal microphthalmia. Am J Obstet Gynecol. 2006;194:1354–1359.
46. Shulman LP, Gordon PL, Emerson DS, Wilroy RS, Elias S. Prenatal
diagnosis of isolated bilateral microphthalmia with confirmation
by evaluation of products of conception obtained by dilation and
evacuation. Prenat Diagn. 1993;13:403–409.
47. Schneider A, Bardakjian TM, Zhou J, et al. Familial recurrence of
SOX2 anophthalmia syndrome: Phenotypically normal mother with
two affected daughters. Am J Med Genet A.
48. Vutova K, Peicheva Z, Popova A, Markova V, Mincheva N, Todorov
T. Congenital toxoplasmosis: Eye manifestations in infants and children. Ann Trop Paediatr. 2002;22:213–218.
49. Turner GM, Twining P. The facial profile in the diagnosis of fetal
abnormalities. Clin Radiol. 1993;47:389–395.
50. Menashe Y, Ben Baruch G, Rabinovitch O, Shalev Y, Katznelson
MBM, Shalev E. Exophthalmus—Prenatal ultrasonic features for
diagnosis of Crouzon syndrome. Prenat Diagn. 1989;9:805–808.
51. Gershoni-Baruch R, Drugan A, Bronshtein M, Zimmer EZ. Roberts
syndrome or “X linked Amelia”? Am J Med Genet. 1990;37:
569–572.
52. Bocino CA, Platt LD, Garber A, et al. Fetal akinesia hypokinesia
sequence: Prenatal diagnosis and intrafamilial variability. Prenat
Diagn. 1993;13:1011–1019.
53. Amaya L, Taylor D, Russell-Eggitt I, Nischal KK, Lengyel D. The
morphology and natural history of childhood cataracts [review].
Surv Ophthalmol. 2003;48:125–144.
54. Katorza E, Rosner M, Zalel Y, Gilboa Y, Achiron R. Prenatal ultrasonographic diagnosis of persistent hyperplastic primary vitreous.
Ultrasound Obstet Gynecol. 2008;32:226–228.
55. DeMyer W, Zeman W, Palmer CG. The face predicts the brain:
Diagnostic significance of median facial anomalies for holoprosencephaly (arhinencephaly). Pediatrics. 1964;34:256–263.
56. Romero R, Pilu G, Jeanty P, Chidini A, Hobbins JC, eds. The face.
In: Prenatal Diagnosis of Congenital Anomalies. East Norwalk, CT:
Appleton & Lange; 1988:81–113.
2008;146A:2794–2798.
57. Khudr G, Olding L. Cyclopia. Am J Dis Child. 1973;125:120–122.
58. Elejalde Br, de Elejalde MM, Hamilton PR, Christenson R, Broekhuizen
F. Prenatal diagnosis of cyclopia. Am J Med Genet. 1983;14:15–19.
59. Toth Z, Csecsei K, Szeifert G, Papp Z. Early prenatal diagnosis of
cyclopia associated with holoprosencephaly. J Clin Ultrasound.
1986;14:550–553.
60. Meizner I, Drawall D, Mazor M, Katz. Sonographic findings in a rare
case of fetal cyclopia. Isr J Med Sci. 1987;23:910–912.
61. Van Allen MI, Ritchie S, Toi A, Fong K, Winsor E. Trisomy 4
in a fetus with cyclopia and other anomalies. Am J Med Genet.
1993;46:193–197.
62. Arakaki DT, Waxman SH. Trisomy D in a cyclops. J Pediatr.
1969;74:620–622.
63. Jaschevatzky OE, Goldman B, Georghiou P, Grunstein S, Pevzner
S. Trisomy D in a cyclops with cardiovascular defects. Acta Obstet
Gynecol Scand. 1976;55:73–76.
64. Taysi K, Tinaztepe K. Trisomy D and the cyclops malformation. Am
J Dis Child. 1972;124:710–713.
65. Mollica F, Pavone L, Nuciforo G, Gorge G. A case of cyclopia: Role
of environmental factors. Clin Genet. 1979;16:69–71.
66. Rolland M, Sarramon MF, Bloom MC. Astomia-agnathiaholoprosencephaly association: Prenatal diagnosis of a new case.
Prenat Diagn. 1991;11:199–203 .
67. Cho FN, Kan YY, Chen SN, Lee TC, Hsu TJ, Hsu PH. Prenatal
diagnosis of cyclopia and proboscis in a fetus with normal chromosome at 13 weeks of gestation by three-dimensional transabdominal
sonography. Prenat Diagn. 2005;25:1059–1060.
68. Pilu G, Reece EA, Romero R, Bovicelli L, Hobbins JC. Prenatal
diagnosis of craniofacial malformations with ultrasonography. Am J
Obstet Gynecol. 1986;155:45–50.
69. Chervenak FA, Tortora M, Mayden K, et al. Antenatal diagnosis of
median cleft face syndrome: Sonographic demonstration of cleft lip
and hypertelorism. Am J Obstet Gynecol. 1984;149:94–97.
70. Shever DM, Shah YG, Wang N, Metlay LA, Wood JR, Jr. Prenatal
diagnosis and subsequent management of a fetus with a 46 XYr (4)
(p15-q35) karyotype. Am J Perinatol. 1991;8:53–55.
71. Trout T, Budorick NE, Pretorius DH, McGahan JP. Significance
of orbital measurements in the fetus. J Ultrasound Med. 1994;13:
937–943.
72. Anderka MT, Lin AE, Abuelo DN, Mitchell AA, Rasmussen SA.
Reviewing the evidence for mycophenolate mofetil as a new teratogen: Case report and review of the literature. Am J Med Genet A.
2009;149A:1241–1248.
73. Farrel SA, Leadman TML, Davidson RG, Caco C. Prenatal diagnosis
of retinal detachment in Walker-Warburg syndrome. Am J Med
Genet. 1987;28:619–624.
74. Monteagudo A, Ayalon A, Mayberry P. Walker-Warburg syndrome: Case report and review of the literature. J Ultrasound Med.
2001;20:419–426.
75. Vohra N, Ghidini A, Alvarez M, Lockwood C. Walker–Warburg
syndrome: Prenatal ultrasound findings. Prenat Diagn. 1993;13:
575–579.
76. Chitayat D, Toi A, Babul R, et al. Prenatal diagnosis of retinal nonattachment in the Walker-Warburg syndrome. Am J Med Genet.
1995;56:351–358.
77. Blin G, Rabbé A, Ansquer Y, Meghdiche S, Floch-Tudal C, Mandelbrot
L. First-trimester ultrasound diagnosis in a recurrent case of WalkerWarburg syndrome. Ultrasound Obstet Gynecol. 2005;26:297–299.
78. Redmond RM, Vaughan JI, Jay M, Jay B. In utero diagnosis of Norrie
disease by unltrasonography. Ophthalmol Pediatr Genet. 1993;14:
1–3.
79. Maat-Kievit JA, Oepkes D, Hartwig NG, Vermeij-Keers C, Van
Kamp IL, Van De Kamp JJP. A large retinoblastoma detected in a
fetus at 21 weeks of gestation. Prenat Diagn. 1993;13:377–384.
80. Salim A, Wiknjosastro GH, Danukusumo D, Barnas B, Zalud I. Fetal
retinoblastoma. J Ultrasound Med. 1998;17:717–720.
81. Singh AD, Black SH, Shields CL, Shields JA. Prenatal diagnosis
of retinoblastoma. J Pediatr Ophthalmol Strabismus. 2003;40:2
22–224.
82. Lau CS, Choy KW, Fan DS, et al. Prenatal screening for retinoblastoma in Hong Kong. Hong Kong Med J. 2008;14(5):391–394.
83. Xu K, Rosenwaks Z, Beaverson K, Cholst I, Veeck L, Abramson
DH. Preimplantation genetic diagnosis for retinoblastoma: The first
reported liveborn. Am J Ophthalmol. 2004;137:18–23.
Chapter 14 The Fetal Eye
425
84. Sueters M, Peek AM, Ball LM, et al. Prenatal detection of orbital
rhabdomyosarcoma. Arch Ophthalmol. 2005;123:276–279.
85. Hingorani M, Mannor G, Vardy SJ, et al. Prenatal diagnosis of orbital
heterotopic brain tissue. J Pediatr Surg. 1997;32:1348–1350.
86. Moon YJ, Hwang HS, Kim YR, Park YW, Kim YH. Prenatally
detected congenital orbital teratoma. Ultrasound Obstet Gynecol.
2008;31:107–109.
87. Abbasi AH, Haj N, Nseir T, Garzozi HJ. Prenatal diagnosis of
dacryocystocele. Eye. 2007;21:1537–1538.
88. Wong RK, VanderVeen DK. Presentation and management of congenital dacryocystocele. Pediatrics. 2008;122:e1108–1112.
89. Yen MT, Tse DT. Congenital orbital cyst detected and monitored by prenatal ultrasonography. Ophthal Plast Reconstr Surg.
2001;17:443–446.
90. Kushner BJ. Congenital nasolacrimal system obstruction. Arch
Ophthalmol. 1982;100:597–600.
91. Harris GJ, DiClementi D. Congenital dacryocystocele. Arch
Ophthalmol. 1982;100:1763–1765.
92. Paul TO, Shepard R. Congenital nasolacrimal duct obstruction:
Natural history and the timing of the optimal intervention. J Pediatr
Opthalmol Strabismus. 1994;31:362–367.
93. Davis WK, Mahoney BS, Carroll BA, Bowie JD. Antenatal sonographic detection of benign dacrocystoceles (lacrimal duct cysts).
J Ultrsound Med. 1987;6:461–465.
94. Alper CM, Chan KH, Hill LM, Chenevey P. Antenatal diagnosis of
congenital nasolacrimal duct cyst by ultrasonography: A case report.
Prenat Diagn. 1994;14:623–626.
95. Walsh G. Dubbins PA. Antenatal sonographic diagnosis of dacryocystocele. J Ultrasound Med. 1994;22:457–460.
96. Sharony R, Raz J, Aviram R, Cohen I, Beyth Y, Tepper R. Prenatal
diagnosis of dacryocystocele: A possible marker for syndromes.
Ultrasound Obstet Gynecol. 1999;14:71–73.
97. Bault JP, Quarello E. Retinal coloboma: Prenatal diagnosis using
a new technique, the “virtual fetal eyeground.” Ultrasound Obstet
Gynecol. 2009;33:495–496.
98. Cross HE, Maumenee AE. Ocular trauma during amniocentesis.
Arch Ophthalmol. 1973;90:303–304.
99. Merin S, Beyth Y. Uniocular congenital blindness as a complication of midtrimester amniocentesis. Am J Ophthalmol. 1980;89:
299–301.
100. Isenberg SJ, Heckenlively JR. Traumatized eye with retinal damage
from amniocentesis. J Pediatr Ophthalmol Strabismus. 1985;22:
65–67.
101. Admoni MM, Ben Ezra D. Ocular trauma following amniocentesis as a cause of leukocoria. J Pediatr Ophthalmol Strabismus.
1988;25:196–197.
102. Naylor G, Roper JG, Willshaw HE. Ophthalmic complications of
amniocentesis. Eye. 1990;4:845–849.
103. Rummelt V, Rummelt C, Naumann GOH. Congenital nonpigmented epithelial iris cyst after amniocentesis: Clinicopathologic
report on two children. Ophthalmology. 1993;100:776–781.
104. Birnholz JC. The development of human fetal eye movement patterns. Science. 1981;213:679–681.
105. Arduini D, Rizzo G, Giorlandino C, Valensise H, Dellacqua S,
Romanini C. The development of fetal behavioral states: A longitudinal study. Prenat Diagn. 1986;6:117–124.
106. Horimoto N, Koyanagi T, Satoh S, Yoshizato T, Nakano H. Fetal
eye movement assessed with real time ultrasonography: Are these
rapid and slow eye movements? Am J Obstet Gynecol. 1990;163:
1480–1484.
107. Nijhuis JG, Prechtl HFR, Martin BR, Jr, Bates RSGM. Are there
behavioral states in the human fetus? Early Hum Develop.
1982;6:177–195.
108. Birnholz JC, Benacerraf BR. The development of human fetal hearing. Science. 1983;222:516–518.
109. Horimoto N, Koyanagi T, Takashima T, Akazawa K, Nakano H.
Changes in pupillary diameter in relation to eye movement and
no eye movement periods in the human fetus at term. Am J Obstet
Gynecol. 1992;167:1465–1469.
110. Righini A, Avagliano L, Doneda C, et al. Prenatal magnetic resonance imaging of optic nerve head coloboma. Prenat Diagn.
2008;28:242–246.
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Chapter 15
FETAL CEREBRAL CIRCULATION
Ritsuko K. Pooh ● Shimon Degani
KEY POINTS
1. Data collected from Doppler velocity recordings
using both spectral and color Doppler mode confirm
the fundamental aspects of the fetoplacental
circulation. Changes in placental vascular resistance,
cardiac contractibility, vessel compliance, and blood
viscosity alter the normal dynamics of fetal cerebral
circulation.
2. Reference values have been established for the main
cerebral vessels. During the last trimester of normal
pregnancies, the values of Doppler waveform indices
decrease in all main cerebral vessels. After birth,
vascular resistance decreases, and later stabilizes.
Cerebral autoregulation persists from fetal to
postnatal life, with low waveform indices in cerebral
vessels of growth-retarded fetuses and neonates.
The low indices indicate decreased cerebrovascular
resistance, representing the redistribution of flow, or
the brain-sparing effect.
3. Combined parameters recorded from different
vascular beds may provide support for the diagnosis
of significant hemodynamic changes and are of
prognostic value in predicting fetal outcome such as
fetal IUFGR and Rh disease.
4. As far as imaging of the vascularization (arterial
and venous) of the prenatal brain, it should be clear
that no brain scan should be considered complete
without looking at its main vessels or at least at
the pericallosal artery on a median section. Should
such a protocol be too complicated to achieve in all
anomaly scans, it is important to scrutinize brain
vascularization in each and every case of suspected
brain anomaly.
5. Three-dimensional power Doppler US technology,
especially combined with high-frequency TVS, as
described in this and other chapters, is the most
preferable noninvasive and reproducible imaging
method to be used. The accurate information about
deviant brain vascularity may help to render proper
obstetric, neurologic, and neurosurgical management.
Recent sonographic advances have contributed to accurate
and reliable visualization of intrauterine vascularity. The
first breakthrough in the assessment of fetal circulation was the Doppler system. Technical developments
in Doppler ultrasound (US) equipment, especially highly
sensitive color Doppler, power Doppler, and bidirectional power Doppler imaging techniques, have made
it possible to study the fetal circulatory system, including cerebral vascularization. Early fetal circulation has
been demonstrated by conventional two-dimensional (2D)
color Doppler since the 1990s.
choroid plexus were depicted and assessed in 1994.
Two-dimensional color/power Doppler combined with
transvaginal sonography (TVS) became a powerful tool
to demonstrate early fetal vascularization.
fetal development is amazingly rapid, and the structure
of the brain changes throughout pregnancy. Introduction
of three-dimensional (3D) power Doppler technology in
the late 1990s enabled visualization of intracranial vessels.
This assessment, combined with TVS, has provided 3D
sonoangiographic images, and adds useful information in
the prenatal evaluation of normal brain development, vascular malformation, and tumoral vascularity.
1
Fine vessels inside the
4 , 5
Embryonal/
6 , 7
2 , 3
DEVELOPMENT OF EMBRYONAL
CEREBRAL CIRCULATION
Vascular endothelial cells cover the entire inner surface
of blood vessels and are influenced by vascular endothelial growth factor (VEGF), which is a potent angiogenic
factor working as an endothelial cell-specific mitogen and
exerting a trophic effect on neurons and glial cells. Both
of these activities are essential during central nervous
system (CNS) vascularization, development, and repair.
In these cells, VEGF expression developmentally regulates and is correlated with angiogenesis, which in turn
responds to the high metabolic demands of the developing fetal brain.
From the beginning of cardiac development, the cranial parts of the truncus arteriosus enlarge and transform
into the aortic sac, which later gives rise to the aortic
branches. After splitting of the truncus arteriosus by
the aorticopulmonal septum, the primoridal aortic sac
8
428
Chapter 15 Fetal Cerebral Circulation
becomes part of the ventral aorta, while a pair of the dorsal
aortae develop independently of the cardiac tube. During
later development, extensive changes occur, leading to
loss of the symmetrical state of these primitive vessels. In
brief, the common aortic artery, along with the first part
of the internal carotid artery (ICA), arises from the third
aortic branch, while the rest of the vessels develop from
the cranial part of the dorsal aorta. The external carotid
artery develops as a cranial part of the third aortic branch,
while the vertebral arteries emerge from the dorsal aorta.
In the development of cerebral fetal veins, the upper cardinal veins play the most important role, draining the blood
from the cranial part of the embryo.
During fetal development (approximately 35 gestational days), the craniocerebral circulation is characterized by temporary connections between the primitive
carotid and the paired dorsal longitudinal neural arteries
(precursors of the vertebrobasilar system). They include
persistent trigeminal, ottic, hypoglossal, and proatlantic
intersegmental arteries. Normal embryonic development
underwrites the regression of all these vessels totally.
Sometimes the regression does not occur, resulting in a
persistent trigeminal artery, which is the most frequent
reason (85% of cases) of primitive carotid-to-basilar artery
anastomoses.
9
NORMAL VASCULARIZATION OF
THE FETAL CENTRAL NERVOUS SYSTEM
It should be said at the outset that the best way to study
fetal circulation during its development is by employing
2D as well as 3D color and power Doppler technologies. Due to their physical limitations, transabdominal
transducers cannot achieve high enough resolution to
accurately display fine vessel anatomy. Therefore, highfrequency transvaginal probes have to be used for the best
results.
Also the use of color and power Doppler should be
used judiciously and sparingly during the first trimester
according to the ALARA (as low as reasonably achievable)
radiation safety suggestion (Title 10, Section 20.103 of the
Code of Federal Regulators (USFNR).
Assessment of cerebral vascularization becomes possible from the seventh postmenstrual week of gestation,
capturing low-velocity flow signals with an obvious absence
of diastolic flow, from the periphery (walls) of the rhombencephalic cavity.
3
At that stage the lateral ventricles are
small evaginations located laterally and rostrally from
the cavity of the diencephalon directly contiguous with
the mesencephalon ( Figure 15–1 ). The isthmus rhombencephali represents the connection to the rhombencephalic
cavity and the future fourth ventricle. At this time of the
evolution, the cavity of the rhombencephalon is the largest brain cavity visible in the embryonic head, as shown in
Figure 15–1 . From 8 postmenstrual weeks of gestation, it
is possible to detect blood flow signals from the ICA and
vertebral artery. At this stage, the rhombencephalic cavity (future fourth ventricle) decreases in size and moves
toward the occipital part. Upon reaching the brain, the two
ICAs turn dorsally and course alongside the diencephalon,
giving off their branches. The ICA and its branches—the
anterior cerebral artery (ACA), the middle cerebral artery
(MCA), and the posterior communicating artery—form a
polygonal-shaped communicating vessel called the circulus arteriosus, or the circle of Willis. The vessels arising
from the circle of Willis supply the blood flow to the entire
brain. Other vessels that form the circle are the vertebral
arteries running between the transverse processes of C2
to C6 and giving a branch called the basilar artery and the
posterior cerebral artery (PCA). The main components
of the circulus arteriosus are present at Carnegie stage 16
(crown-rump [C-R] length of 10 mm, or 38 days postconception), and the circle is complete with Carnegie stage 16
(see Chapter 1 ). Arteries originating from the vertebral
arteries are important for the supply of the cerebellum and
brainstem. Within the symmetrical cerebellar hemispheres,
it is possible to visualize the intracerebellar arteries.
Blood flow signals from the intracerebellar arteries can be
obtained from the ninth postmenstrual week of gestation,
AB
Figure 15–1. Early embryonal vascularity at 7 postmenstrual weeks. (A) Sagittal sonographic image of the embryo. (B) Bidirectional power Doppler
image on the same section.
AB
Chapter 15 Fetal Cerebral Circulation
MCA
ICA
C
CCA
429
Figure 15–2. Early embryonal vascularity at 9 postmenstrual weeks.
(A) Sagittal sonographic image of the fetus. (B) Three-dimensional (3D)
power Doppler image of fetal vascularity with surface display mode.
(C) 3D power Doppler angiographic image of the vascular system.
as shown in Figure 15–2 . After the ninth postmenstrual
week, the cerebellar superior, anteroinferior, and posterior
arteries can be detected and separated from other cerebral
arteries. These arteries are characterized by low to moderate impedance to blood flow. Three-dimensional power
Doppler imaging presents the early vascular anatomy at
the base of the skull with branches evolving laterally to the
mesencephalon and cephalic flexure.
10
With advancing gestational age, a progressive increase
in blood flow velocity is noted for all cerebral arteries. Between the 9th and 10th postmenstrual weeks, the
diastolic velocity component begins to emerge, but it is
inconsistently present. From the 11th postmenstrual week,
the end-diastolic blood-flow component of the velocity
waveform begins to be consistently present. The posterior
lateral choroidal artery derives from the PCA, whereas
the lateral choroidal artery derives from the MCA and
the ICA. Blood flow signals from the choroid plexus are
obtained during the 9th and 10th postmenstrual weeks of
gestation as subtle color and pulsed Doppler signals at the
inner edge of the choroid plexus of the lateral ventricle.
This developmental period is also the time of active neurogenesis. Choroid plexus vascularity during weeks 9 and 10
has two typical features: the presence of prominent venous
blood flow signals and the absence of diastolic flow.
2 , 11
In
parallel, at this early age the cranial venous system, important for brain drainage, develops gradually. The venous
circulation drains the blood into the dural sinuses, which
meet in the confluence of the sinuses (torcular herophili)
at the occipital pole of the skull, from where the blood flow
drains into the jugular veins. As stated before, color/power
Doppler and pulsed Doppler enable imaging and evaluation of the carotid artery
8
and cerebral arterial blood flows.
The MCA has been of particular interest to clinicians and
clinical researchers alike and is therefore the objective of
Doppler measurements and studies as the most important
representative blood vessel of the brain. This interest is
evident even at present, as measurements of blood flow
profiles have stayed in daily clinical practice. The MCA
is the largest branch of the ICA, supplying ∼80% of the
A
Figure 15–3. Vascular structure of normal 12 postmenstrual week
brain by 3D power Doppler angiographic rendering. (A) Coronal power
Doppler image of common carotid arteries (CCA), internal carotid arteries (ICA), and their branches. (B) Axial or horizontal 3D power Doppler
angiographic image obtained from the parietal direction. The circle of
Willis (asterisk) is clearly visualized. MCA, middle cerebral arteries.
B
cerebral hemisphere. In middle and late pregnancy, the
greater wings of the sphenoid bone, between the anterior
and middle fossae, are good reference points for locating the MCA. It runs laterally in the sylvian fissure as a
continuation of the intracranial carotid artery. This vessel
consists of four segments—M1, M2, M3, and M4—and
sends branches to the corpus striatum, the internal capsule, and the leuticulostriate nucleus. The preferable site
for Doppler assessment is the M1 segment, as it maintains
a more constant diameter. It then continues to cruise
posteriorly over the surface of the insula and the inferior
frontal gyrus.
In Figure 15–3 , the bilateral common carotid arteries,
the ICA and the basilar arteries, were imaged in the coronal plane, as seen on the left side of the figure, while the
circle of Willis and two MCAs were demonstrated from
the parietal view using 3D power Doppler reconstructed
imaging, seen on the right of Figure 15–3 , at 12 postmenstrual weeks’ gestation. The ACA and its branches can be
demonstrated using the sagittal plane from the late first
trimester. From the late first or early second trimester,
the MCA, ACA, and their branches can be demonstrated
by transvaginal 3D power Doppler ( Figure 15–4 ). In the
second trimester, the MCA is also easy visible, and its
peak systolic velocity (PSV) values increase from the 22nd
to 38th postmenstrual week.
12
Figure 15–5 shows the
median 2D/3D bidirectional power Doppler images by
TVS/transfontanelle sonography of the ACA, callosomarginal artery, and their branches. Figure 15–6 shows serial,
consecutive tomographic US images of coronal and sagittal sections of the above arteries. If a more accentuated
impression of the brain vessels is sought, 3D rendering