Holoprosencephaly

A rare complex brain malformation characterized by incomplete cleavage of the prosencephalon, and affecting both the forebrain and face and resulting in neurological manifestations and facial anomalies of variable severity.

Epidemiology

Prevalence is estimated to be 1/10,000 live and still births and 1/250 conceptuses, with worldwide distribution.

Clinical description

Three classical forms of holoprosencephaly (HPE) of increasing severity are described based on the degree of anatomical separation: lobar, semi-lobar and alobar HPE. Milder subtypes include midline interhemispheric variant and septopreoptic HPE. There is, however, a continuous spectrum of abnormal separation of the hemispheres that extends from aprosencephaly/atelencephaly, the most severe end of the spectrum, to microform HPE, a less severe midline defect without the typical HPE brain characteristics. There is significant inter- and intrafamilial clinical variability across this spectrum. In most cases, there is a correlation between the severity of the facial anomalies and the brain defect (except in cases of mutation in the ZIC2 gene). In decreasing severity, the main craniofacial features are cyclopia, proboscis, premaxillary agenesis, median or bilateral cleft lip/palate, coloboma, retinal dysplasia, choanal stenosis, pyriform sinus stenosis, hypotelorism, solitary maxillary median incisor (SMMI) or even normal face. Severe forms are often fatal and mortality is correlated with the severity of brain malformation and associated defects. In surviving children, a wide range of associated manifestations are reported: developmental delay, hydrocephalus, motor impairment, spasticity, feeding difficulties and oromotor dysfunction, epilepsy, hypothalamic dysfunction. Endocrine disorders due to pituitary defects such as central diabetes insipidus are frequent.

Etiology

HPE is due to incomplete cleavage of the prosencephalon between the 18th and 28th day of gestation. The etiology is typically genetic and often oligogenic; however, environmental factors during this period (maternal diabetes or hypocholesterolemia during gestation) may contribute. HPE may also be associated with certain syndromes or chromosomal abnormalities (such as Smith-Lemli-Opitz syndrome, Hartsfield Syndrome and trisomy 13). In isolated HPE, at least 20 genes have been implicated: major genes include SHH (7q36), ZIC2 (13q32), SIX3 (2p21), GLI2 (2q14), FGF8 (10q24) and FGFR1 (8p11) in addition to more than 15 minor genes. The major common effect of the identified pathogenic mutations is the impairment of SHH activity leading to disruption of the ventral midline of the brain, and interference with the early stages of forebrain and eye development. SHH-dosage is crucial in the disease mechanism and might determine disease severity.

Diagnostic methods

Most severe cases are detected by systematic ultrasound scan and magnetic resonance imaging (MRI) during pregnancy or after birth. At the other end of the spectrum, diagnosis is based on clinical features.

Differential diagnosis

Differential diagnosis includes anencephaly, severe congenital hydrocephalus, Walker-Warburg syndrome, large interhemispheric cyst, otocephaly and other midline defects, as well as syndromic and chromosomal-related forms.

Antenatal diagnosis

Due to the high clinical and genetic variability, prenatal diagnosis is based on ultrasound scans and MRI rather than on molecular diagnosis, and may be useful in mothers with diabetes and those with a family history of HPE. Some parents of a child with a structural unbalanced chromosome rearrangement (e.g., deletion, duplication) have a balanced chromosome rearrangement and should be offered chromosome analysis by chorionic villus biopsy or amniocentesis.

Genetic counseling

Genetic counseling (GC) is strongly recommended for affected families; it is particularly complex and requires thorough clinical evaluation and family history, with close attention to possible risk factors (especially maternal diabetes), microform findings in relatives, and associated signs. If a genetic etiology is established in a proband, specific counseling for recurrence risk is indicated. In non-syndromic HPE, all modes of inheritance have been described; however, most cases are complex with digenic or oligogenic inheritance.

Management and treatment

Treatment is symptomatic and supportive, and requires a multidisciplinary approach.

Prognosis

Prognosis depends on severity and the associated complications.

* European Reference Network