The surgery and management of children who have congenital malformations of the skull and meninges require multidisciplinary care and long-term follow-up by multiple specialists in birth defects. The high definition of three-dimensional CT and MRI allows precise surgery planning of reconstruction and management of associated malformations. The reconstruction of meningoencephaloceles and craniosynostosis are challenging procedures that transform the child’s appearance. The embryology, clinical presentation, and surgical management of these malformations are reviewed.
Congenital malformations of the skull and meninges occur as often as 1 in 10,000 births. Although meningoencephaloceles and craniosynostosis are apparent at birth, dermal sinus tracts may escape detection until much older ages. Arachnoid cysts are common incidental findings of neuroimaging of the sinuses or after trauma. The foundations of surgical repair of these malformations are based on their embryology and anatomy. Optimum management of children requires close cooperation between a pediatric neurosurgeon and multiple specialists involved with congenital defects. This article reviews the embryology, clinical presentation, and surgical management of these malformations.
Embryology
Beginning on gestational day 15, gastrulation initiates the complex tissue migration converting the primitive bilaminar embryo into three cell layers. The primitive streak begins as a thickening of the superficial ectoderm that deepens rostrally to form Hensen’s node. Groove formation along the length of the primitive streak further deepens at Hensen’s node to direct surface cell migration and interposition between the ectoderm and endoderm, forming the paraxial mesoderm. Further cell migration cephalad between the mantles of mesoderm, the endoderm below, and the ectoderm above forms the notochordal process. Extension of the notochord cephalad is limited by the prochordal plate and caudally by the cloacal membrane .
The notochord begins as a solid core of cells but cavitates from the primitive pit, forming the notochordal canal. During intercalation, the notochordal canal fuses with the ventral endoderm opening this canal into the yolk sac. On gestation day 17, the neurenteric canal (of Kovalevsky) penetrates from Hensen’s node through the notochord communicating the amniotic cavity to the inner yolk sac. This transient channel is closed during excalation, with infolding of the notochordal plate in a cranial to caudal direction. The endoderm is reconstituted as a continuous cell layer, and the notochordal canal disappears. Mesoderm condenses about the true notochord, inducing formation of the neural plate and the vertebral bodies. With continued embryo growth, Hensen’s node and the primitive streak are displaced caudally toward the sacrococcygeal region .
At stage XII of embryologic development, the cranial and cervical notochord separates from the adjacent neural tube, marking the site of the synchondrosis between the future sphenoid and occipital bones. Condensation of adjacent mesoderm eventually differentiates into the major bones of the skull base. Preliminary chondrification begins during stage XVI in the skull base and the body of the sphenoid bone. By stage XX, the hypoglossal nerve passes through a chondrified foramen, lateral to the foramen magnum. Vascularization of the cephalic neural tube begins at stages XII and XIII.
The bones of the calvarium originate from multiple ossification centers that surround the developing embryonic brain. Bone enlargement is induced by the expansion of brain volume and size. The development of sutures is initiated by approximation of the cranial bones. The sutures provide a dynamic mechanical union between adjacent skull bones, serving as the site of bone resorption and deposition. Fibrous desmocranium develops into an outer periosteum and an inner dural layer that fuses with the dura propria of mesoderm origin. Premature suture closure is often associated with anomalies of the cranial base. There is mixed evidence suggesting that skull base changes may be primary malformations or secondary to suture closure or both .
Flanked by mesoderm, the notochord induces growth of the neural plate and the vertebral bodies. The superficial ectoderm is destined to form brain, spinal cord, and skin, whereas endoderm matures into the gastrointestinal and respiratory tracts. The mesoderm guides maturation of bone marrow, connective tissue, skeletal muscle, and bone; a remnant of the notochord persists as the nucleus pulposis of the intervertebral disc.
During gestational days 18 through 27, the neural tube is formed by primary neurulation. Closure of the neural groove begins at the rostral neuropore in the region of the future hindbrain and continues toward the caudal neuropore. The anterior neuropore develops into the optic chiasm, septum pellucidum, lamina terminalis, and the rostrum of the corpus callosum. The posterior neuropore corresponds with the S2 level of the spinal cord. The superficial cutaneous ectoderm and neuroectoderm are rigidly adherent until neural tube closure has been completed. These layers separate during dysjunction, allowing dorsolateral mesoderm migration. The notochord and caudal end of the developing neural tube blend into a skin-covered, undifferentiated caudal cell mass.
Neuronal architecture develops about vacuoles within this primitive streak during secondary neurulation or canalization . The vacuoles coalesce into a tubular structure that fuses with the more rostral neural tube. Regression within the caudal cell mass begins before canalization has been completed. There is condensation of the distal neural lumen, forming the cauda equina and filum terminale.
Meningeal development begins at stage XIV, and by stage XVI, there is a membranous roof surrounding the central cavity of the developing brain. During fetal development, arachnoid is the final of the meninges to differentiate. On rupture of the rhombic roof, cerebrospinal fluid (CSF) invaginates into the layers of the perimedullary mesh, stimulating differentiation between the subarachnoid and the subdural spaces. Pia matter evolves later from this inner mesh. This layer separation appears at a 180-mm crown-rump embryo length, at approximately 15 weeks’ gestation. Incomplete separation of the mesh creates septations within the subarachnoid space. Dura develops from mesoderm cells of the sclerotome and develops continuous with the cells of the intervertberal discs. Dura circumferentially surrounds the developing brain and spinal cord by 80 mm crown-rump length.
Arachnoid cysts may develop when alterations of CSF flow lead to rupture of the primitive arachnoid septations. A diverticulum may invaginate, entrapping CSF in a noncirculating compartment. Another hypothesis is arachnoid splitting during delamination from the overlying dura. Arachnoid cysts may be associated with agenesis of the corpus callosum and anomalies of the dura venous sinuses.
The formation of dermal sinuses may reflect incomplete dysjunction . Focal incomplete separation of the cutaneous ectoderm from the neural ectoderm during the fourth week of fetal development retains adherence of these layers . Altered dysjunction can lead to the dermal sinus extension from the subcutaneous tissues to the intramedullary or subarachnoid space. Although the lumbosacral region is the most common location for dermal sinuses, they may occur anywhere along the developing nervous system, from the top of the intergluteal fold to the occiput or nasion. Disorder of notochord formation, with sagittal splitting of the spinal cord and hindbrain and persistence of dorsal cutaneoendomesenchymal fistula, has also been suggested as a alternative mechanism of dermal sinus formation .
The sinus tract is lined by columns of squamous epithelium encased by dermal and neuroglial tissue. Within the tract, nerve or ganglion cells, fat, cartilage, and fibrovascular meningeal remnants may be found . Nearly 60% of dermal sinus tracts enter the subarachnoid space. Cranial dermal sinus tracts of the posterior skull frequently extend subtorcular into the posterior fossa, and intracranial cysts may grow to considerable size before diagnosis.
Dermoid and epidermoid tumors may arise within focal expansions along the tract in approximately half of all dermal sinuses . These tumors are frequently encountered within the subarachnoid space, arising from congenital rests of cells derived from the caudal cell mass or mesoderm . Dermoid histology is most common; epidermoids are seen in 13%, and teratoma and malignant transformations are unusual.
Incomplete mesoderm condensation into the space between the separating neural and surface ectoderm may contribute to encepahlocele formation. With limited development of the overlying cartilage and bone, neural tissue and the meninges protrude and migrate adjacent to the skin. Based on this hypothesis, the defects within the herniated neural tissue may be secondary changes. Other mechanisms for encephalocele formation include malformations of the anterior neuropore and altered ossification within the skull base. Several genes including sonic hedgehog may be linked with encephalocele formation.
Craniosynostosis
Premature suture closure occurs in approximately 1 in 40,000 births. Sagittal suture closure is most common (about 60%), followed by unilateral or bilateral craniosynostosis of the coronal suture (25%). Approximately 15% of children have trigonocephaly from premature metopic suture closure, whereas only 2% to 3% of cases involve closure of the lambdoid suture. Most craniosynostosis is sporadic; a history of suture anomalies is detected in only 8% of coronal craniosynostosis and 2% of sagittal X-linked suture closure. Hydrocephalus and intellectual impairment is rare in isolated single-suture craniosynostosis, in contrast to Apert’s, Pfeiffer’s, and other craniofacial syndromes.
There are many primary and secondary etiologies of craniosynostosis. These etiologies include teratogens such as aminopterin, dilantin, retinoic acid, and valproic acid. Other causes include shunted hydrocephalus, hyperthyroidism, rickets, and the mucopolysaccharidoses. Numerous chromosomal anomalies are linked with craniosynostosis . When craniosynostosis accompanies a chromosomal anomaly, the phenotype of a craniofacial syndrome is always present. Autosomal dominant and recessive inheritance patterns have been identified.
Children who have dysmorphic craniofacial features and unusual skull shapes are typically referred for neurosurgical evaluation at very young ages. Premature fusion of the sagittal suture locks the biparietal skull dimension. Directed by the growth and expansion of the brain, there is compensatory growth of the adjacent coronal and lambdoid sutures, producing elongation and scaphocephaly. In a similar fashion, increased growth of the sagittal and coronal sutures adjacent to unilateral coronal craniosynostosis produces contralateral forehead asymmetry with brachycephaly. Expanding on Virchow’s description of suture growth, Delashaw and colleagues , recognized the compensatory growth of adjacent sutures and bones, predicting the calvarium deformities encountered with craniosynostosis. Orbital dystocia and asymmetry is most common with unilateral and bilateral coronal suture closure. In severe cases of multiple-suture synostosis, there is insufficient orbital volume to accommodate the globe, and vision-threatening proptosis requires urgent surgical repair.
Since the American Academy of Pediatrics recommended the supine sleeping position for infants in the late 1980s, there has been an epidemic of occipital positional plagiocephaly. This acquired deformity has been estimated to occur in 5% to 10% of all children younger than 12 to 18 months. There is a parallelogram skull deformity, with contralateral occipital prominence and ipsilateral forehead asymmetry. The ipsilateral pinna is displaced anterior-inferior, in contrast to posterior-inferior displacement with true lambdoid synostosis. Whereas surgical reconstruction is warranted for correction of lambdoid synostosis, occipital plagiocephaly responds to repositioning, head rotation, and helmet orthoses .
Radiology of craniosynostosis
Suture anatomy is well defined by plain skull radiographs, which may be the sole imaging warranted for diagnosis and surgical planning of sagittal suture fusion . Among a group of 85 children who had sagittal craniosynostosis reported by Boop and colleagues , there were unexpected intracranial findings on brain CT, including a benign tumor in 5%, prompting the investigators’ recommendation for preoperative CT. In a recent review conducted by Agrawal and colleagues , the requirement for any imaging of isolated sagittal craniosynostosis was questioned. Three-dimensional (3-D) CT assists preoperative simulation of planned osteotomies and reconstruction ( Fig. 1 A, B). Postoperative 3-D CT imaging allows comparison with preoperative scans to assess the volumetric changes in the skull base and calvarium.
Surgery technique
Many techniques for craniofacial reconstruction have been developed. Dependent on brain growth for remodeling, linear strip craniectomy or synostectomy was the most common reconstruction technique for many years. Rapid bone regeneration was common, and caustic solutions or polyethylene applied to bone edges were modifications to restrict bone growth. The goals of contemporary reconstruction techniques are more extensive bone removal with active remodeling and reconstruction of the calvarium. Spiral osteotomies allow radical widening of the biparietal dimension in sagittal craniosynostosis and the posterior skull reconstruction in repair of lambdoid closure. The pi procedure was developed for immediate correction of the scaphocephalic head shape by active shortening of the elongated anterior-posterior skull dimension ( Fig. 2 A, B) . Subtemporal decompression and barrel-stave osteotomies widen the biparietal dimension of the skull base. Repair of metopic and coronal suture craniosynostosis advances an orbital margin bandeau with forehead reconstruction.
Radical forehead advancement procedures were pioneered by Tessier and colleagues . These techniques have benefited from the parallel advances in pediatric anesthesia. Rigid bone fixation is appropriate in the child older than 3 years; however, reconstruction in younger children must accommodate the final stages of brain growth and expansion, which is accomplished with floating islands of bone sutured to the dura or the use of resorbable plate and screw fixation .
Minimally invasive endoscopic reconstruction techniques were first developed by Jiminez and Barone . These techniques complete a wide-strip craniectomy of the involved suture through two small incisions. The endoscope provides sufficient exposure for the completion of barrel-stave osteotomies and craniectomy that extends to the skull base. Intraoperative blood loss and scalp swelling is minimized, and hospital length of stay is shortened. A dynamic cranial orthosis is necessary post surgery for nearly a year to maintain optimum head shape.
Irrespective of reconstruction technique, the risks of synostosis repair are low, with rare complications related to infection, blood transfusion, or orbital, dural, or cortical injury. Air embolism is very rare despite operative positions that frequently place the head above the heart . Most synostosis surgery achieves an extraordinary transformation of the shape of the calvarium and skull base. Long-term follow-up is recommended to monitor skull growth, vision, and neurologic milestone development . There is a small group of children requiring second-stage reconstruction.
Craniosynostosis
Premature suture closure occurs in approximately 1 in 40,000 births. Sagittal suture closure is most common (about 60%), followed by unilateral or bilateral craniosynostosis of the coronal suture (25%). Approximately 15% of children have trigonocephaly from premature metopic suture closure, whereas only 2% to 3% of cases involve closure of the lambdoid suture. Most craniosynostosis is sporadic; a history of suture anomalies is detected in only 8% of coronal craniosynostosis and 2% of sagittal X-linked suture closure. Hydrocephalus and intellectual impairment is rare in isolated single-suture craniosynostosis, in contrast to Apert’s, Pfeiffer’s, and other craniofacial syndromes.
There are many primary and secondary etiologies of craniosynostosis. These etiologies include teratogens such as aminopterin, dilantin, retinoic acid, and valproic acid. Other causes include shunted hydrocephalus, hyperthyroidism, rickets, and the mucopolysaccharidoses. Numerous chromosomal anomalies are linked with craniosynostosis . When craniosynostosis accompanies a chromosomal anomaly, the phenotype of a craniofacial syndrome is always present. Autosomal dominant and recessive inheritance patterns have been identified.
Children who have dysmorphic craniofacial features and unusual skull shapes are typically referred for neurosurgical evaluation at very young ages. Premature fusion of the sagittal suture locks the biparietal skull dimension. Directed by the growth and expansion of the brain, there is compensatory growth of the adjacent coronal and lambdoid sutures, producing elongation and scaphocephaly. In a similar fashion, increased growth of the sagittal and coronal sutures adjacent to unilateral coronal craniosynostosis produces contralateral forehead asymmetry with brachycephaly. Expanding on Virchow’s description of suture growth, Delashaw and colleagues , recognized the compensatory growth of adjacent sutures and bones, predicting the calvarium deformities encountered with craniosynostosis. Orbital dystocia and asymmetry is most common with unilateral and bilateral coronal suture closure. In severe cases of multiple-suture synostosis, there is insufficient orbital volume to accommodate the globe, and vision-threatening proptosis requires urgent surgical repair.
Since the American Academy of Pediatrics recommended the supine sleeping position for infants in the late 1980s, there has been an epidemic of occipital positional plagiocephaly. This acquired deformity has been estimated to occur in 5% to 10% of all children younger than 12 to 18 months. There is a parallelogram skull deformity, with contralateral occipital prominence and ipsilateral forehead asymmetry. The ipsilateral pinna is displaced anterior-inferior, in contrast to posterior-inferior displacement with true lambdoid synostosis. Whereas surgical reconstruction is warranted for correction of lambdoid synostosis, occipital plagiocephaly responds to repositioning, head rotation, and helmet orthoses .
Radiology of craniosynostosis
Suture anatomy is well defined by plain skull radiographs, which may be the sole imaging warranted for diagnosis and surgical planning of sagittal suture fusion . Among a group of 85 children who had sagittal craniosynostosis reported by Boop and colleagues , there were unexpected intracranial findings on brain CT, including a benign tumor in 5%, prompting the investigators’ recommendation for preoperative CT. In a recent review conducted by Agrawal and colleagues , the requirement for any imaging of isolated sagittal craniosynostosis was questioned. Three-dimensional (3-D) CT assists preoperative simulation of planned osteotomies and reconstruction ( Fig. 1 A, B). Postoperative 3-D CT imaging allows comparison with preoperative scans to assess the volumetric changes in the skull base and calvarium.
