Holoprosencephaly Imaging

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Holoprosencephaly Imaging

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 Holoprosencephaly denotes an incomplete or absent division of the embryonic forebrain (prosencephalon) into distinct lateral cerebral hemispheres. [1, 2, 3, 4, 5]

DeMyer historically and roughly categorized holoprosencephaly into 3 types (from most severe to least severe) [6] :

Alobar holoprosencephaly

Semilobar holoprosencephaly

Lobar holoprosencephaly

In alobar holoprosencephaly (shown in the image below), there is a complete absence of midline forebrain division, resulting in a monoventricle and fused cerebral hemispheres.

Semilobar holoprosencephaly is characterized by an incomplete forebrain division, resulting in partial separation of the cerebral hemispheres, typically posteriorly.

In lobar holoprosencephaly (seen in the image below), there is complete ventricular separation, with focal areas of incomplete cortical division or anterior falcine hypoplasia present.

Distinctive midline facial malformations occur in most cases. Typical facial anomalies are correlated with the degree of holoprosencephaly and have prognostic importance. [1, 2] From most severe to least severe, these include the following: (1) cyclopia, in which a single, midline, fused eye exists in a single orbit below a proboscis; (2) ethmocephaly, in which ocular hypotelorism is present with an interorbital proboscis; (3) cebocephaly, in which ocular hypotelorism is present with a single-nostril nose; (4) ocular hypotelorism and midline clefting; and (5) ocular hypotelorism and bilateral clefting.

More subtle facial dysmorphic features may also be present. These include a flat nasal bridge and tip; a single, midline, upper incisor; a bifid uvula; absent nasal bones and nasal septum; and congenital nasal pyriform aperture stenosis (decreased width of the nasal pyriform aperture at the level of the interior meatus).

Microcephaly is the rule, and macrocephaly, if present, is suggestive of hydrocephalus.

Virtually all surviving individuals with the more severe forms of holoprosencephaly have some developmental delay, often persisting as mental retardation. In general, this finding is directly correlated with the severity of holoprosencephaly.

Also not uncommon are seizures, hypotonia and/or hypertonia, extrapyramidal features, such as dystonia and/or chorea; hypothalamic and brainstem dysfunction leading to autonomic dysfunction and swallowing difficulties; pituitary dysfunction, which can manifest as partial or complete panhypopituitarism with resultant endocrine deficiencies; and feeding difficulties, which can lead to aspiration pneumonia and failure to thrive.

Active research into the pathophysiology of holoprosencephaly has revealed multiple teratogenic and genetic causes (chromosomal and single gene); further genetic characterization is ongoing.

The imaging study of choice for the diagnosis and classification of holoprosencephaly is cranial magnetic resonance imaging (MRI). [7, 8, 9] The next best imaging modalities are ultrasonography and cranial computed tomography (CT) scanning. [1, 2, 10, 11, 12, 13, 14] Ultrasonography can be limited in cases of microcephaly if there is a very small fontanelle. Transcranial ultrasonography, however, can be performed through the calvaria, at times using the thinner temporal bones. Often this technique requires a transducer of lower frequency, resulting in better penetration, albeit at the loss of some near-field resolution.

Prenatal evaluation by means of transabdominal or transvaginal ultrasonography can be used to identify most cases of alobar or semilobar holoprosencephaly. Prenatal MRI can be done in cases in which the infant’s head is not easily accessible at the time of ultrasonographic evaluation or in cases in which the anatomy is not satisfactorily delineated at prenatal ultrasonography.

Prenatal ultrasonography is not a reliable method for diagnosing mild forms of holoprosencephaly, such as lobar holoprosencephaly, because of its high false-negative rate. In addition, prenatal ultrasonography often cannot distinguish between alobar holoprosencephaly and semilobar holoprosencephaly. A transabdominal ultrasonographic diagnosis of holoprosencephaly before 16 weeks’ gestation is difficult.

Craniofacial defects associated with holoprosencephaly that may be detected on plain radiographs include a single, fused orbit; orbital hypotelorism; abnormal nasal bone formation; facial clefts; and a single, midline, central incisor.

Changes apparent on plain radiography are nonspecific and are insufficient to make the diagnosis of holoprosencephaly.

Not all individuals with holoprosencephaly have craniofacial abnormalities that are detectable on plain radiography. However, holoprosencephaly is in the differential diagnosis whenever these associated anomalies are found.

On CT scan images, alobar holoprosencephaly results in a horseshoe-shaped monoventricle, an absent interhemispheric fissure, fused thalami, an absent falx, agenesis of the corpus callosum, an absent septum pellucidum, and absent olfactory bulbs.

Semilobar holoprosencephaly is characterized by partial ventricular differentiation, but with a single ventricular cavity, a partial interhemispheric fissure and falx (posterior-ventral axis), partial or incomplete formation of the corpus callosum, and a variable degree of thalamic fusion. The olfactory bulbs are often absent. The abnormality is more severe anteriorly, with partial cleavage and lateral differentiation occurring posteriorly. In patients with semilobar holoprosencephaly, the posterior portion of the corpus callosum is present, and the more anterior portion, where failure of cleavage has occurred, is absent.

Lobar holoprosencephaly occurs with partial fusion of the frontal lobe, with an otherwise normally formed interhemispheric fissure, lateral ventricular formation, variable and incomplete absence of the anterior corpus callosum and/or septum pellucidum, and separate thalami. The olfactory tracts are present.

The middle interhemispheric fusion variant appears as incomplete cleavage of the posterior frontal and parietal lobes and, often, incomplete cleavage of the basal ganglia and thalami. The body of the corpus callosum is absent in the area where cleavage has failed to occur. [15]

CT scans can establish a diagnosis of holoprosencephaly by providing images of brain anatomy. CT scanning is best suited for imaging the bony structure of the skull.

However, CT scanning exposes the patient to ionizing radiation and is therefore relatively contraindicated in the prenatal diagnosis.

CT scanning provides less detail of the brain parenchyma than MRI does, and it does not provide good images of the posterior fossa and brainstem. Therefore, some cases of mild holoprosencephaly and associated central nervous system (CNS) anomalies can be missed on CT scans.

Cranial MRI is the diagnostic imaging modality of choice in cases of holoprosencephaly.

Alobar holoprosencephaly results in a horseshoe-shaped monoventricle, an absent interhemispheric fissure, fused thalami, an absent falx, agenesis of the corpus callosum, an absent septum pellucidum, absent olfactory bulbs, abnormal cerebral cortex, and migration anomalies. The MRI characteristics of alobar holoprosencephaly are demonstrated in the images below.

Semilobar holoprosencephaly is characterized by partial ventricular differentiation, but with a single ventricular cavity, a partial interhemispheric fissure and falx (posterior-ventral axis), partial or incomplete formation of the anterior corpus callosum, and a variable degree of thalamic fusion. The olfactory bulbs are often absent.

Lobar holoprosencephaly (seen in the image below) occurs with partial fusion of the frontal lobe, with an otherwise normally formed interhemispheric fissure, lateral ventricular formation, variable and incomplete absence of the anterior corpus callosum and/or septum pellucidum, and separate thalami. The olfactory tracts are present.

The middle interhemispheric fusion variant appears as incomplete cleavage of the posterior frontal and parietal lobes and incomplete cleavage of the basal ganglia and thalami. The body of the corpus callosum is absent, coincident with the site of failure of cerebral separation. [15]

Fetal MRI may yield false-positive or false-negative results if the study is not performed according to established protocols and if the images are not interpreted by an experienced individual. Fetal activity can significantly degrade the images and may need to be circumvented by repeated sequences. Single-shot fast spin-echo (SS-FSE) MRI techniques can also often circumvent this problem.

At prenatal ultrasonography, primary CNS findings include the following: (1) single, sickle-shaped or horseshoe monoventricle; (2) absent midline echo due to the absence of an interhemispheric fissure, falx, corpus callosum, and septum pellucidum; (3) thin cortical rim; (4) single, fused thalamus; (5) microcephaly; and (6) ventriculomegaly/hydrocephalus.

Associated craniofacial ultrasonographic findings include the following: (1) ocular hypotelorism or cyclopia, (2) proboscis or abnormal nasal bone formation, and (3) cleft lip and/or palate (midline or bilateral).

Postnatally, alobar holoprosencephaly shows a single ventricle, fused thalami, and a thin, usually poorly differentiated cortical mantle. A dorsal cyst or ventricular remnant may also be detected.

Semilobar holoprosencephaly is detected by identifying the partial cleavage of the occipital horns and the presence of a posterior falx and a posterior portion of the corpus callosum. Anteriorly, there is typically fusion of the ventricles and of the hemispheres, with concomitant absence of the corpus callosum and of the septum pellucidum.

Lobar holoprosencephaly is a continuum. In some patients, the ultrasonographic images show fusion of the anterior horns and of portions of the frontal lobes. The mildest forms of lobar holoprosencephaly may be manifested only by absence of the septum pellucidum.

Sonograms of the middle interhemispheric fusion variant demonstrate normal cleavage anteriorly and posteriorly, with fusion of the hemispheres and absence of the body of the corpus callosum in the posterior, frontal, and parietal regions. [15]

Reportedly, cases of alobar holoprosencephaly have been detected as early as 9-14 weeks’ gestation (and often detected at 18-20 weeks on routine anatomic scans), semilobar holoprosencephaly has been detected by 13-20 weeks’ gestation, and lobar holoprosencephaly has been detected by 21 weeks’ gestation with the use of transvaginal ultrasonography. Conventional transabdominal ultrasonography cannot achieve this degree of early detection.

Fetal MRI should be considered to confirm and further classify cases of holoprosencephaly.

Prenatal ultrasonography is not a reliable method of diagnosing mild forms of holoprosencephaly, such as lobar holoprosencephaly, because of its high false-negative rate. In addition, prenatal ultrasonography often cannot distinguish between alobar holoprosencephaly and semilobar holoprosencephaly. Transabdominal ultrasonographic diagnosis of holoprosencephaly before 16 weeks of gestation is difficult.

A false-positive diagnosis of holoprosencephaly has been reported in cases of hydrocephalus, hydranencephaly, arachnoid or porencephalic cysts, Dandy-Walker malformations with ventriculomegaly, septo-optic dysplasia, and other CNS malformations.

Angiography is not indicated, because it is unnecessary in establishing a diagnosis of holoprosencephaly. In the past, however, in cases of alobar and semilobar holoprosencephaly, an azygous anterior cerebral artery running over the cerebral surface has been documented by angiography to correlate somewhat with the degree of holoprosencephaly.

Cohen HL, Sivit CJ, eds. Holoprosencephaly. Fetal and Pediatric Ultrasound: A Casebook Approach. New York, NY: McGraw-Hill; 2001. 12-6.

Muenke M, Beachy PA. Holoprosencephaly. Scriver CR, Beaudet AL, Sly WS, et al, eds. The Metabolic & Molecular Bases of Inherited Disease. 8th ed. New York, NY: McGraw-Hill; 2001. 6203-30.

Leoncini E, Baranello G, Orioli IM, et al. Frequency of holoprosencephaly in the International Clearinghouse Birth Defects Surveillance Systems: Searching for population variations. Birth Defects Res A Clin Mol Teratol. 2008 Jun 19. epub ahead of print. [Medline].

Dubourg C, Bendavid C, Pasquier L, et al. Holoprosencephaly. Orphanet J Rare Dis. 2007 Feb 2. 2:8. [Medline]. [Full Text].

Golden JA. Towards a greater understanding of the pathogenesis of holoprosencephaly. Brain Dev. 1999 Dec. 21(8):513-21. [Medline].

DeMyer W, Zeman W, Palmer CG. The face predicts the brain: diagnostic significance of median facial anomalies for holoprosencephaly (arhinencephaly). Pediatrics. 1964 Aug. 34:256-63. [Medline].

Herman-Sucharska I, Urbanik A. [MRI of fetal central nervous system malformations] [Polish]. Przegl Lek. 2007. 64(11):917-22. [Medline].

Sonigo PC, Rypens FF, Carteret M, Delezoide AL, Brunelle FO. MR imaging of fetal cerebral anomalies. Pediatr Radiol. 1998 Apr. 28(4):212-22. [Medline].

Barkovich AJ, Maroldo TV. Magnetic resonance imaging of normal and abnormal brain development. Top Magn Reson Imaging. 1993 Spring. 5(2):96-122. [Medline].

Kim MS, Jeanty P, Turner C, Benoit B. Three-dimensional sonographic evaluations of embryonic brain development. J Ultrasound Med. 2008 Jan. 27(1):119-24. [Medline]. [Full Text].

Wilson RD, Chitayat D, McGillivray BC. Fetal ultrasound abnormalities: correlation with fetal karyotype, autopsy findings, and postnatal outcome–five-year prospective study. Am J Med Genet. 1992 Nov 15. 44(5):586-90. [Medline].

McGahan JP, Nyberg DA, Mack LA. Sonography of facial features of alobar and semilobar holoprosencephaly. AJR Am J Roentgenol. 1990 Jan. 154(1):143-8. [Medline]. [Full Text].

Winter TC, Kennedy AM, Woodward PJ. Holoprosencephaly: a survey of the entity, with embryology and fetal imaging. Radiographics. 2015 Jan-Feb. 35 (1):275-90. [Medline].

Gondré-Lewis MC, Gboluaje T, Reid SN, Lin S, Wang P, Green W, et al. The human brain and face: mechanisms of cranial, neurological and facial development revealed through malformations of holoprosencephaly, cyclopia and aberrations in chromosome 18. J Anat. 2015 Sep. 227 (3):255-67. [Medline].

Lewis AJ, Simon EM, Barkovich AJ, et al. Middle interhemispheric variant of holoprosencephaly: a distinct cliniconeuroradiologic subtype. Neurology. 2002 Dec 24. 59(12):1860-5. [Medline].

David H Tegay, DO, FACMG Associate Professor and Chair, Department of Medicine, NYIT College of Osteopathic Medicine; Director, Genetics Division, Department of Pediatrics, Nassau University Medical Center

David H Tegay, DO, FACMG is a member of the following medical societies: American College of Medical Genetics and Genomics, American College of Osteopathic Internists, American Osteopathic Association, Federation of American Societies for Experimental Biology, American Society of Human Genetics

Disclosure: Nothing to disclose.

Harris L Cohen, MD, FACR Chairman, Department of Radiology, Professor of Radiology, Pediatrics, and Obstetrics and Gynecology, University of Tennessee Health Science Center College of Medicine; Radiologist-in-Chief, LeBonheur Children’s Hospital; Emeritus Professor of Radiology, The School of Medicine at Stony Brook University

Harris L Cohen, MD, FACR is a member of the following medical societies: American College of Radiology, American Institute of Ultrasound in Medicine, Radiological Society of North America, Society for Pediatric Radiology, Association of Program Directors in Radiology, Society of Radiologists in Ultrasound

Disclosure: Nothing to disclose.

Mark Rosovsky, MD Attending Radiologist, Advanced Radiology Associates, Bridgeport Hospital

Mark Rosovsky, MD is a member of the following medical societies: American Society of Neuroradiology, Radiological Society of North America

Disclosure: Nothing to disclose.

Bernard D Coombs, MB, ChB, PhD Consulting Staff, Department of Specialist Rehabilitation Services, Hutt Valley District Health Board, New Zealand

Disclosure: Nothing to disclose.

Marta Hernanz-Schulman, MD, FAAP, FACR Professor, Radiology and Radiological Sciences, Professor of Pediatrics, Department of Radiology, Vice-Chair in Pediatrics, Medical Director, Diagnostic Imaging, Vanderbilt Children’s Hospital

Marta Hernanz-Schulman, MD, FAAP, FACR is a member of the following medical societies: American Institute of Ultrasound in Medicine, American Roentgen Ray Society

Disclosure: Nothing to disclose.

Eugene C Lin, MD Attending Radiologist, Teaching Coordinator for Cardiac Imaging, Radiology Residency Program, Virginia Mason Medical Center; Clinical Assistant Professor of Radiology, University of Washington School of Medicine

Eugene C Lin, MD is a member of the following medical societies: American College of Nuclear Medicine, American College of Radiology, Radiological Society of North America, Society of Nuclear Medicine and Molecular Imaging

Disclosure: Nothing to disclose.

Michael A Bruno, MD, MS, FACR Professor of Radiology and Medicine, Pennsylvania State University College of Medicine; Director, Radiology Quality Management Services, The Penn State Milton S Hershey Medical Center

Michael A Bruno, MD, MS, FACR is a member of the following medical societies: American College of Radiology, American Roentgen Ray Society, Association of University Radiologists, Radiological Society of North America, Society of Nuclear Medicine and Molecular Imaging, Society of Skeletal Radiology

Disclosure: Received royalty from Oxford Press for book author/editor & reviewer; Received royalty from Elsevier Press for book author / editor.

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