Developmental malformations present the most frequent reasons for collaboration between pediatric surgeons and neurosurgeons, for at least 4 reasons. First, the juxtaposition of neuroectoderm and endoderm during early embryonic development produces a number of malformations involving both neural and gastrointestinal tissues (such as combined spina bifida) in ways that require a collaborative effort to repair. Second, certain malformations of the gastrointestinal system (such as imperforate anus or certain gastrointestinal duplications) or chest (such as neurenteric cysts of the posterior mediastinum) may serve as markers for additional developmental malformations involving the nervous system. Third, certain central nervous system abnormalities (such as myelocystocele or spinal lipomas) may be mistaken for malformations involving other organ systems (such as sacrococcygeal teratoma). Finally, seemingly innocuous malformations involving the face (such as nasal dermal sinuses) or back (such as midline skin tags, hemangiomata, or hairy patches) that may be referred to a pediatric surgeon for removal may have occult intracranial extension or serve as sentinel markers of important underlying central nervous system malformations that, if not properly addressed, may lead to complications involving the central nervous system. Although these relationships cannot always be predicted in advance, knowing the developmental anatomy of the nervous system and understanding the ways in which the neuroectoderm and endoderm can interact will eliminate a number of unpleasant surprises.
Normal Development of the Nervous System
It is very helpful to have a basic understanding of early neural development. The human embryo at 2 weeks of gestation is a bilaminar structure containing an epiblast and hypoblast (Fig. 76-3A). During the third week, cells in the epiblast migrate toward the mid-line primitive streak and ingress through the primitive groove to form the endoderm (these cells displace the hypoblast cells laterally) and the intervening mesoderm; the remaining epiblast cells form the ectoderm (Fig. 76-3A). These cell movements, termed gastrulation, convert the embryo from a bilaminar to a trilaminar structure containing ectoderm, mesoderm, and endoderm.
Normal human gastrulation. A. Prospective endodermal and mesodermal cells of the epiblast migrate through the primitive groove; remaining epiblast cells will become the neuroectoderm and cutaneous ectoderm. B. Prospective notochordal cells located in Hensen node ingress through the primitive pit (the rostral end of the primitive streak) to become the notochordal process. (From Dias MS, Walker ML. The embryogenesis of complex dysraphic malformations: a disorder of gastrulation? Pediatr Neurosurg 1992;18:229–253.)
Cells at the rostral end of the primitive streak in the Hensen node ingress through the primitive pit (the cranial end of the primitive groove) and become the notochordal process (Fig. 76-3B). The notochordal process initially is hollow, consisting of a ring of cells radially arranged about a central lumen (the notochordal canal), which, in turn, is in communication with the primitive pit (Fig. 76-4A). During the third week of embryogenesis, the notochordal process fuses (intercalates) with the underlying endoderm for a period of about 3 days; during this period, the notochordal canal is contiguous with both the amnion and the yolk sac and creates a “through and through” hole in the embryo termed the primitive neurenteric canal (Fig. 76-4B). At the end of this period, the notochordal canal separates (excalates) from the endoderm, and the primitive neurenteric canal is obliterated (Fig. 76-4C).
Notochordal development. A. The notochordal process contains a central lumen (the notochordal canal), which is continuous with the amnionic cavity through the primitive pit. B. During intercalation, the notochordal process fuses with the underlying endoderm; the communication of the amnion with the yolk sac is called the neurenteric canal. C. During excalation, the notochord rolls up and separates from the endoderm; the neurenteric canal is obliterated. (From Dias MS, Walker ML. The embryogenesis of complex dysraphic malformations: a disorder of gastrulation? Pediatr Neurosurg 1992;18:229–253.)
The ectoderm is subdivided into neuroectoderm (the forerunner of the central nervous system), which occupies the medial ectoderm, and cutaneous ectoderm (the future integument), to which the neuroectoderm is bound along its lateral and rostral borders. During the fourth week of embryogenesis, the neuroectoderm undergoes a complex series of morphologic changes that convert the flattened neuroectoderm (or neural plate) to a closed tubular structure (the neural tube) through a process called primary neurulation (Fig. 76-5A, B, and C). The flattened neural plate undergoes midline bending to form the neural groove; elevation and convergence of the lateral portions of the neural plate (the neural folds) and their fusion in the midline produce the closed neural tube. As the neural folds fuse, the cutaneous ectoderm separates and becomes the overlying skin. Abnormalities of neural tube closure often produce additional cutaneous abnormalities such as midline hemangiomata, hairy patches, dimples, or appendages that serve as markers for the underlying abnormality of the neural tube. Neurulation begins in the hindbrain or upper spinal cord and proceeds both cranially and caudally; the last areas to close are the anterior and posterior neuropores, which are located at the lamina terminalis (just anterior to the optic chiasm) and the second sacral spinal cord segment, respectively.
Photomicrographs of human neuroepithelium during neurulation. A. The neuroepithelium is a pseudostratified columnar epithelium. The neural groove is well seen in the midline overlying the notochord, and the neural folds are slightly elevated. B. Later stage shows further elevation of the neural folds about the midline neural groove. C. Still later stage shows a nearly closed neural tube; the cutaneous ectoderm (the future integument) is still attached to the neural folds. Ot, otic placode. (From O'Rahilly R, Müller F. The Embryonic Human Brain. An Atlas of Developmental Stages. New York: Wiley-Liss; 1994.)
The more caudal portions of the neural tube (the spinal cord caudal to the second sacral segment and the filum terminale) are formed from the caudal cell mass (the caudal embryonic remnant of the primitive streak and Hensen node) through a different process termed secondary neurulation (Fig. 76-6). Multipotent cells in the caudal cell mass that are destined to form the caudal nervous system, the mesenchyme of the lower sacrum and coccyx, and the caudal embryonic pole are in juxtaposition with both the posterior notochordal and hindgut endodermal cells (the portion of endoderm that is destined to form anorectal structures). During secondary neurulation, cells of the caudal cell mass become radially arranged into multiple “tubules”; these structures later coalesce to form the secondary neural tube and eventually fuse with the neural tube formed from primary neurulation. The juxtaposition of the caudal cell mass and the underlying hindgut endoderm produces a variety of congenital abnormalities that may involve both anorectal structures and the caudal neuraxis.
Secondary neurulation in chick embryos. A. Cells of the caudal cell mass (ccm), located at the neural tube formed from primary neurulation (1° NT) form multiple independent vesicles. B. These vesicles fuse to form a secondary neural tube. C. The secondary neural tube then fuses with the primary neural tube (NC, notochord). (From Dias MS, McLone DG. Spinal dysraphism. In: Weinstein SL, ed. The Pediatric Spine: Principles and Practice. New York: Raven Press; 1994.)
Beginning at about the sixth gestational week and continuing into postnatal life, the neural tube undergoes several morphogenetic changes, which ultimately result in an “ascent of the conus medullaris”; this is accomplished through 2 distinct mechanisms. Before embryonic day 54, the caudal end of the neural tube undergoes a number of histoanatomic changes collectively referred to as retrogressive differentiation, becoming more slender and fibrous and eventually being transformed into the filum terminale. Beyond embryonic day 54, differential growth of the vertebral column relative to the neural tube results in a progressive length discrepancy so that the conus medullaris ascends during development (Fig. 76-7). The conus in the majority of neonates (particularly those beyond 3 months of age) lies opposite or cranial to the disc space between the first and second lumbar vertebrae (the L1-2 disc space). A spinal cord that ends more caudally, with the conus at or below the L1-2 disc space, is generally considered to be radiographically tethered.
Ascent of the conus medullaris. A–C. Throughout prenatal development, the caudal spinal cord comes to lie at progressively more cranial levels as a result of retrogressive differentiation before embryonic day 54, and differential growth of the spinal cord and vertebral column. At birth (D), the cord normally lies opposite or craniad to the disc space between the first and second lumbar vertebrae. A conus, which is more caudally located, is considered to be tethered.
Although brief, this overview of early embryology will provide a background for a more complete understanding of congenital neural malformations. For a more complete discussion of normal and abnormal neural development, the interested reader is referred to several recent references.
Congenital Craniospinal Malformations
Most contemporary texts divide dysraphic malformations into those that are open (eg, anencephaly, myelomeningocele, and meningocele), and those that are occult (eg, spinal lipoma, split cord malformations, neurenteric cysts, dermal sinus tracts, myelocystocele, thickened filum terminale, and caudal agenesis). Although superficially attractive, this classification scheme is confusing in that many of the “occult” malformations have clinically apparent midline skin markers (hemangiomas, sinuses, appendages, or tufts of hair) that, for the astute clinician, serve as markers for the underlying spinal cord anomaly. We have instead recently begun to emphasize a classification based on reputed embryogenetic mechanisms (Table 76-1).
Table 76-1Embryogenetic Classification of Spinal Developmental Malformations |Favorite Table|Download (.pdf) Table 76-1 Embryogenetic Classification of Spinal Developmental Malformations
|Malformation ||Reputed Embryogenetic Mechanism |
|Myelomeningocele ||Segmental failure of primary neurulation |
|Lipomyelomeningocele ||Premature dysjunction (separation of the neuro-and-cutaneous ectoderm) |
|Dermal sinus ||Incomplete dysjunction |
|Split spinal cord malformations ||Failure of midline axial integration during gastrulation |
|Thickened filum terminate ||Disordered development of caudal cell mass |
|Sacral agenesis ||Failure of caudal cell mass development |
Myelomeningocele is the most common dysraphic malformation compatible with life and occurs with a frequency of 1 in 1200–1400 live births. Myelomeningocele represents a localized failure of primary neurulation—a portion of the neural tube has failed to properly close, and the neural tissue (or placode) therefore remains attached to the surrounding skin (Fig. 76-8) and is, by definition, exposed on the back of the infant (ie, there is no such thing as a “closed myelomeningocele”). Myelomeningoceles are usually cystic appearing because of the accumulation of spinal fluid beneath the placode. Although some reserve the term myeloschisis for a large or flat lesion, myelomeningoceles and myeloschisis both represent the same embryonic problem, failure of primary neurulation. The use of 2 terms to describe essentially the same disorder is confusing, and it has been suggested that the term myeloschisis be discarded.
Photo of a child with a myelomeningocele. The placode is located in the central portion of the malformation and is circumferentially connected along its lateral borders (arrows) with dystrophic skin.
Although the pediatric surgeon is not usually involved initially, many children with myelomeningocele eventually develop problems for which the pediatric surgeon may be called on to assist with management. Many patients with myelomeningocele require shunt placement and complications of shunt operations (see Fig. 76-8) are the most common reasons for consultation. Assistance with vascular access for placement of ventriculoatrial shunts, access to the pleural space for ventriculopleural shunts, or surgical exposure to the gallbladder for ventriculogallbladder shunts may be requested. Children with multiple abdominal adhesions or distorted anatomy from multiple previous operations or infections may require lysis of adhesions during shunt placement. Some children with myelomeningocele and chronic constipation may benefit from creation of a cecostomy or appendicostomy for bowel lavage. Placement of gastrostomy tubes and fundoplication may be required for complications of swallowing dysfunction and/or gastroesophageal reflux as a result of brainstem dysfunction secondary to the Chiari malformation. These procedures may also be complicated by the presence of the ventricular shunt.
A potential therapeutic intervention offered by highly specialized pediatric surgeons and maternal fetal medicine physicians at select centers involves the prenatal repair of the defect. In a randomized study, prenatal repair was shown to improve hydrocephalus and hindbrain herniation, reduce the need for ventriculoperitoneal shunting, and improve distal neurologic function in some patients. While there was some maternal morbidity reported, the results are encouraging for avoiding some of the serious complications faced by the myelomeningocele patient population.
It is important to understand and to convey accurate and reliable information when dealing with children with myelomeningoceles. Most children with isolated myelomeningoceles (ie, those without associated major anomalies of other organs) survive to adulthood, and their life expectancy is nearly normal (although a few children die each year, usually from unrecognized shunt failure or complications of treatment). Eighty percent have normal intelligence; although 60% of these have some learning disability (verbal scores are better than performance scores, and math and problem solving are particularly difficult). Hydrocephalus requiring a ventricular shunt is present in 85% of children but bears little relationship to intelligence. Sixty percent of preadolescents are capable of ambulating, either with or without assistance (although this number drops during adolescence), and about 80% are “socially continent” (meaning they are dry, although many perform clean intermittent catheterization).
Myelomeningocele is a static disease, and any deterioration in a child with myelomeningocele should prompt a search for an underlying cause. Unfortunately, most children with myelomeningocele experience 1 or more episodes of clinical deterioration sometime during their lives. By far, the most common cause of deterioration is a shunt malfunction, which can present in a bewildering number of ways. Nowhere else in pediatric neurosurgery is clinical judgment so important (and misjudgment so treacherous) as in the evaluation of a child with myelomeningocele and suspected shunt malfunction. In addition to the usual triad of headache, nausea, and vomiting, these children may present with neck or back pain (especially at the myelomeningocele closure site), seizures (either new in onset or a change in a preexisting pattern of seizures), significant changes in behavior or school performance, swallowing or other evidence of hindbrain dysfunction, changes in upper or lower extremity strength, coordination, balance, or tone, changes in urinary or bowel habits, and scoliosis or other orthopedic deformities. Finally, as discussed above, the child with shunt malfunction may have papilledema without any symptoms. In short, shunt malfunction in this population can be the root cause for any deterioration, and the clinician should always check the shunt before entertaining any other treatment options. If any doubt exists about shunt function, the shunt should be explored operatively before any other procedures are undertaken.
Other causes of deterioration in children with myelomeningoceles include hindbrain and spinal cord dysfunction from the Chiari malformation and/or syringomyelia (occurring in 15% to 20% of children) and spinal cord tethering (occurring in about one-third of children). The Chiari malformation (Fig. 76-9) refers to a constellation of brain malformations, part of which involves a descent of the cerebellar vermis, caudal brainstem, and the fourth ventricle through the foramen magnum at the skull base and into the rostral spinal canal, which may produce symptoms by compressing the brainstem and rostral spinal cord. Although it is radiographically present in nearly every child with a myelomeningocele, only about 15% to 33% of children develop significant symptoms from the Chiari malformation. Symptoms and signs most commonly (up to 90% of symptomatic children) develop during the first year of life and generally consist of lower cranial nerve dysfunction (swallowing abnormalities, regurgitation, recurrent aspiration pneumonia, hoarseness or vocal cord palsy, obstructive or central apnea); upper-extremity weakness; ataxia, dyscoordination, or gait disturbance; or scoliosis.
Sagittal T1-weighted MRI showing a Chiari malformation and syringomyelia in a child with myelomeningocele. The midline vermis (curved arrow) and medulla are located within the spinal canal below the level of the foramen magnum. Two syringomyelic cavities (small arrows) occupy the cervical and thoracic spinal cord.
Those children with symptomatic Chiari malformations should undergo a cervicomedullary decompression of the brainstem and upper spinal cord with a dural patch graft to create additional space for the spinal cord and descended cerebellar and brainstem tissue. The laminae at all vertebral levels overlying the descended cerebellar tonsils are removed, the dura is opened widely, and a graft of pericranium, cadaver dura, bovine pericardium, or other material is sutured circumferentially to the dural opening. Although a small portion of the occipital bone at the foramen magnum is often removed, a wide bony removal is not necessary because children with Chiari II malformations already have a large foramen magnum. Similarly, opening the fourth ventricular outlets, plugging the obex (the opening from the fourth ventricle to the central canal of the spinal cord), and other maneuvers are probably of little additional value in most cases and significantly increase the operative risk.
Postoperatively, pain, sensorimotor deficits, and cerebellar function improve in the majority, but swallowing dysfunction and/ or vocal cord palsies, particularly if severe, may not improve significantly, and fundoplication, gastrostomy feeding tubes, and tracheostomies may be necessary to prevent pulmonary aspiration.
Syringomyelia (Fig. 76-9) refers to a cystic collection of spinal fluid within the substance of the spinal cord and is present in 20% to 40% of children with myelomeningocele. Treatment is generally reserved for those whose collections are either very large or causing symptoms. Syringomyelia produces symptoms by stretching and compressing the adjacent spinal cord tissue. Symptoms may include progressive weakness in upper and/or lower extremities, loss of sensation, back or radicular pain, or scoliosis. Changes in bowel or bladder function are rare.
Syringomyelia is generally treated with a laminectomy over the largest portion of the syrinx, opening the syrinx either in the midline raphe or, alternatively, dorsolaterally at the dorsal root entry zone (taking care to avoid the cervical enlargement if possible), and placing a shunt tube from the syrinx cavity to either the peritoneal (syringoperitoneal) or pleural (syringopleural) space. Cervicomedullary decompression of the Chiari malformation is less frequently successful in treating syringomyelia in children with Chiari II malformations.
Spinal cord tethering is identified radiographically by an abnormally low-lying position of the spinal cord terminus, below the L1–2 disc space. Again, spinal cord tethering is radiographically evident in virtually every child with myelomeningocele but produces symptoms in only about a third. The pathophysiology of tethering has been studied both in humans and in animal models by Yamada and colleagues; the stretching of the spinal cord produces changes in spinal cord blood flow, which, in turn, lead to ischemia and changes in mitochondrial oxidative metabolism in the caudal spinal cord.
Symptoms and signs of spinal cord tethering may include back and/or leg pain, weakness or loss of leg function, deteriorating gait, deterioration in bowel or bladder function, and increasing scoliosis or other lower-extremity orthopedic deformities such as pes cavus and equinovarus deformities. Symptoms are thought to arise because the repaired myelomeningocele placode is scarred at the site of the previous closure and cannot ascend with the child's growth and movements; unrecognized associated malformations such as split cord malformations or thickened filum terminale (see below) may provide additional sources of tethering. Surgery is reserved for those children with symptomatic tethering and involves exploration and untethering of the placode and any associated tethering elements from the dura and surrounding structures such that the spinal cord lies free within the thecal sac. The dura is closed primarily or with a dural patch graft. A number of synthetic grafts have been tried to prevent retethering, but none has met with significant long-term success.
Although the radiologic abnormalities of the tethered cord, Chiari malformation, and syringomyelia are present radiographically in many children with myelomeningocele, the mere presence of any of these malformations does not, by itself, suggest the need for treatment. Rather, treatment is reserved for children having evidence of clinical deterioration.
Spinal Lipomas (Lipomyelomeningocele)
Spinal lipomas are the most frequent of the closed congenital spinal cord malformations, accounting for 35% of skin-covered lumbosacral masses. An associated subcutaneous fatty mass (Fig. 76-10A, B, and C) is present in 70% of patients. Rarely, the mass is mistaken for a sacrococcygeal teratoma, although spinal lipomas are almost always more rostrally located in the mid- or upper sacrum. Infrequently, they may involve the thoracic or cervical spine. Other cutaneous markers may include midline lumbosacral hemangiomas, dimples, skin tags, or appendages. The subcutaneous component of the lipoma virtually always extends through a dorsal defect in the spine (often, but not always, between dysplastic laminae) and ends within the intramedullary portion of the spinal cord (Fig. 76-10C). Rarely, the lipoma may be purely intradural, having no subcutaneous component, but still tethers the spinal cord to the dura. Spinal lipomas are thought to arise through premature separation (dysfunction) of the neural tube from the cutaneous ectoderm (skin); this allows mesenchymal cells access to the inside of the neural tube, where they are induced to form fat. Lipomas that originate caudal to the second sacral spinal cord segment (from neural tube derived from secondary neurulation) are thought to arise through a different, as yet undefined, mechanism involving the caudal cell mass, sometimes in association with disorders of cloacal derivatives (urogenital system and hindgut, see below).
Spinal lipoma. A. Photograph of a child with a spinal lipoma. A subcutaneous fatty mass is located on the sacrum above the gluteal cleft. A small hemangioma is evident. B. Sagittal T1-weighted MRI scan shows the fatty mass extending to the spinal canal. The spinal cord (arrows) is low lying. C. Intraoperative photograph shows the fatty mass extending down to, and contiguous with, the spinal cord (arrows). Several spinal nerve roots are evident ventrolateral to the lipoma.
Spinal lipomas, as with all of the congenital spinal cord malformations, produce signs and symptoms of spinal cord dysfunction because of spinal cord tethering at the level of the malformation. Signs and symptoms of tethering include back and/or leg pain; progressive sensorimotor deficits; urologic changes (incontinence, difficulties initiating a urinary stream, frequent bladder infections, or changes on urodynamic studies suggestive of a neurogenic bladder) or defecatory difficulties; orthopedic abnormalities of the feet such as pes cavus, equinovarus deformities, hammer toes, or asymmetric feet; and scoliosis. Current thinking is that most children with spinal lipomas will eventually deteriorate because of tethering, and operation is recommended as soon as the malformation is identified, preferably before the child becomes symptomatic.
Lipomas are readily visible as hyperintense lesions on T1-weighted images (Fig. 76-10B). The spinal cord is low lying, consistent with tethering. The preoperative evaluation includes a formal assessment of lower extremity muscle function (preferably a manual muscle test), a urologic evaluation including urodynamic studies, and an orthopedic assessment of lower-extremity and spinal deformities. Surgery involves excising the lipoma, isolating its underlying attachment with the dorsal spinal cord, and untethering the spinal cord. Most pediatric neurosurgeons also excise some part of the lipoma within the spinal cord substance. It should be emphasized that simply excising the subcutaneous lipoma without addressing its relationship to the underlying spinal cord is not adequate treatment.
The outcome is generally excellent when the lesion is dealt with prophylactically; in a series of 71 asymptomatic patients by McLone and colleagues, none were made worse by surgery, and 66 (93%) remained clinically stable at long-term follow-up. In contrast, among 87 children operated on at the time of clinical deterioration, 2 suffered operative complications, 26% improved (only 11.5% returned to normal), and 51% were stable at long-term follow-up; at long-term follow-up, 41% deteriorated in a delayed fashion and required further untethering operations.
Dermal sinus tracts are thought to represent incomplete dysjunction of the neural tube from the cutaneous ectoderm during neurulation. As a result, a tract of cutaneous tissue remains attached to the nervous system. The lumbosacral dermal sinus tract often extends deep to the ostium, through or between the lamina(e) immediately beneath (Fig. 76-11), penetrates the dura, and ascends within the thecal sac to end on the dorsal aspect of the spinal cord at the level of the posterior neuropore (the second sacral spinal cord level), just above the tip of the conus medullaris. In addition to tethering the spinal cord, dermal sinus tracts can cause symptoms and signs through at least 3 other mechanisms. First, they can serve as a portal of entry for bacteria, leading to recurrent infections (bacterial meningitis or spinal abscess). Second, desquamation of epithelial cells and debris from the dermoid tumor can produce an intense inflammatory response, resulting in aseptic meningitis. Third, dermoid tumors can develop within the spinal cord or canal and compress the spinal cord.
Photograph of a dermal sinus tract (curved arrow) in the sacral region. The gluteal cleft (small arrows) is abnormally deviated toward the left.
Dermal sinus tracts almost always have some associated cutaneous marker, usually the tract itself, which produces a lumbosacral dimple. Dermal sinus tracts are usually easy to differentiate from the benign coccygeal dimple, which is present in about 4% of normal infants. As its name implies, the benign coccygeal dimple is located at or just above the tip of the coccyx within the gluteal cleft. The tip of the coccyx is readily palpated deep to the dimple. In contrast, the dermal sinus tract is located higher, in the “flat” of the lumbosacral area, well rostral to the coccyx and almost always cranial to the end of the gluteal cleft (Fig. 76-11). Dermal sinus tracts may be irregular, surrounded by heaped-up areas of skin or small dermal masses, or associated with cutaneous hemangiomas, skin tags, or tufts of hair within the ostium. Abnormal or asymmetric forking of the gluteal cleft is common; the dermal sinus tract may be located at the end of one fork. Finally, dermal sinus tracts may be associated with focal neurologic deficits, a neurogenic bladder, or orthopedic deformities. Benign coccygeal dimples are never associated with any of these findings.
An MRI of the lumbar spine will show the spinal cord to be tethered. Dermoid tumors, if present, may be seen within the thecal sac or spinal cord parenchyma but may be isointense to spinal fluid or spinal cord and therefore difficult to visualize. Unfortunately, dermal sinus tracts are not always visible on MRI, and the absence of a visible tract does not exclude a connection. If the lesion appears clinically suspicious, especially if the conus is abnormally low, the malformation should be explored regardless of whether a tract is visible on MRI. The tract is followed down to the underlying spine, a laminectomy is performed, and the tract is followed to its terminus at the conus medullaris; any associated dermoid tumors are also removed.
Rarely, the “tug of war” between cutaneous and neuroectoderm may instead be won by the cutaneous ectoderm, pulling the neuroectoderm toward the skin and producing a myelomeningocele manqué. The involved neuroectoderm usually is in the form of dorsal roots that leave the underlying spinal cord, penetrate the dura, and end either in the subcutaneous tissues or even within the skin. The skin overlying the malformation is usually somewhat thinned and scarified and has been referred to as a “cigarette burn” (Fig. 76-12); it is sometimes painful and tender. The skin malformation again serves as a marker for the underlying spinal cord malformation; rather than simple excision of the skin lesion, the entire malformation should be dealt with to treat spinal cord tethering. Again, for both dermal sinus tracts and myelomeningoceles and manqué acute, simply removing the cutaneous component without addressing the underlying spinal cord malformation is not sufficient.
Myelomeningocele manqué. Photograph shows a scarified area of skin. At surgery, nerve roots extended from the skin lesion to the spinal cord.
Dermal sinus tracts may also be visible at the cranial end of the neural tube, most commonly either frontally (frontonasal sinus tracts) or in the occiput (occipital sinus tracts); they rarely occur in a midline parietal location. Dermal sinus tracts between the nasion and the midparietal region may penetrate the bone of the skull and end perilously close to the sagittal sinus but should never have an intradural extension. The reason for this is embryologic—the explosive growth of the cerebral hemispheres after neural tube closure should sweep any malformation involving neural tube closure posterior to the area just behind the vertex.
Frontonasal dermal sinus tracts typically begin along the dorsum of the nose anywhere between the tip and the nasion (Fig. 76-13) and travel between the skin and nasal cartilage to end at or near the anterior skull base (Fig. 76-14). Although they often appear innocuous and may end harmlessly in the extracranial space, some sinuses extend intracranially through a tiny defect in the anterior skull base near the foramen cecum and serve as a portal of entry for intracranial infection (meningitis or brain abscess), or as a source of intracranial dermoid tumors. The occipital dermal sinus tract similarly can have intracranial extension into the supratentorial compartment, the posterior fossa, or both, with intracranial complications.
Frontonasal dermal sinus tract in an infant. The ostium of the tract is located at the glabella (curved arrow).
Normal frontonasal development (A–C) and the embryology of frontonasal dermal sinus tracts (D). A. During normal embryogenesis, the fonticulus nasofrontalis forms between the frontal and nasal bones; the prenasal space forms between the nasal bone and nasal cartilage. B. A tongue of dura extends through the foramen cecum toward the midline nasal skin. C. Later, this tongue of dura is obliterated, and the anterior cranial base is formed; the foramen cecum remains as a vestige of this embryonic tract. D. Abnormal dysjunction during closure of the anterior neuropore leaves a tract of cutaneous ectoderm between the commissural plate and the midline nasal skin. Formation of the anterior frontobasal structures results in a tract whose cutaneous opening may be located at the fonticulus nasofrontalis or anywhere along the dorsum of the nose, and that extends through the foramen cecum, between the two halves of a bifid crista galli, and along the anterior cranial base; in rare instances, the tract extends all the way to the commissural plate. (Adapted from Sessions RB. Nasal dermal sinuses: new concepts and explanations. Laryngoscope 1982;92(Suppl 29):1–28.)
The radiographic workup of cranial dermal sinus tracts should include both enhanced cranial MRI and CT scans with bone windows and coronal views through the anterior skull base. The frontonasal dermal sinus tract and/or associated dermoid tumors are best visualized on MRI scans with gadolinium-enhanced sagittal and coronal views, but a small bony defect may be visible only on coronal CT scans with bone windows, even though an intracranial abnormality on MRI cannot be found. Unfortunately, some intracranial connections may not be visible even with high-resolution imaging studies. As with the lumbosacral dermal sinus tracts, all suspicious lesions should be explored even if radiographic studies are negative. These lesions are best approached in a combined fashion with a pediatric surgeon, otolaryngologist or plastic surgeon, and a pediatric neurosurgeon. If there is a known intracranial extension, the entire tract is explored and removed, either in a combined extra- and intracranial procedure or in 2 separate procedures (with the intracranial portion usually being performed first). If there is no visible intracranial extension, the extracranial tract may be excised locally, and the tract followed toward the skull base, with the pediatric neurosurgeon on stand-by; an intracranial exploration may be necessary if intracranial extension is found at the time of surgery.
Split Cord Malformations, Neurenteric Cysts, the Split-Notochord Syndrome (Combined Spina Bifida), and other Complex Dysraphic Malformations
A number of spinal cord malformations involve concomitant anomalies of the gastrointestinal system, posterior mediastinum, and/or retroperitoneum as neurenteric cysts or certain enteric or bronchial duplications, diverticula, or fistulaes. The key to understanding these malformations lies in properly appreciating the embryonic relationship between the developing neural tube and the endoderm during early development.
Most of these malformations involve a split-cord malformation (SCM) in which the spinal cord is split or clefted over a portion of its length. The terms diastematomyelia and diplomyelia were used in the past but have generated a great deal of confusion; these terms have therefore been largely supplanted by the common term SCM. Two types of SCMs are recognized. Type I lesions are double dural sac malformations in which both the spinal cord and dural sac are split, and there is an extradural bony or fibrocartilaginous spur interposed between the 2 thecal sacs (Fig. 76-15A). Type II malformations are single dural sac malformations in which the spinal cord, but not the thecal sac, is clefted, and both hemicords are therefore contained within a common dural sac (Fig. 76-15B). Although the earlier literature suggested that the type II malformations did not contain any tethering elements, at surgery, fibrous bands of tissue (analogous to the bony or cartilaginous spurs of the type I malformations) are usually found between the 2 hemicords. In addition, both types contain aberrant nerve roots that exit from the medial aspects of one or both hemicords and end blindly on the midline mesenchymal elements, which can additionally tether the spinal cord. Both types of malformations therefore contain tethering elements, which can produce neurologic deterioration. Associated congenital spinal cord malformations such as lipomas, dermal sinus tracts, and thickened filum terminale may be present and present additional tethering elements.
Split-cord malformations (SCM). A. Axial metrizamide myelogram of a type I SCM shows 2 hemicords (small arrows), each ensheathed in its own dural sac, and separated by a midline bony spike (curved arrow). B. Axial T1-weighted MRI scan of a type II SCM shows 2 hemicords (black arrows) within a single dural sac. A midline tethering band is not visible in the MRI but was found at surgery.
An associated enteric malformation may also be present and may be the feature that prompts medical attention. The most common malformation is a posterior mediastinal (foregut) or retroperitoneal “dorsal enteric cyst” often (in about 50% of cases) associated with an adjacent clefted vertebral body (“butterfly” vertebra) or other vertebral anomaly. The enteric cyst may contain either enteric tissues (gastric, small intestinal, or colonic) or bronchial tissues (in the mediastinal cases), suggesting that these malformations arise before the normal separation of the gut from the tracheobronchial tree. Posterior mediastinal cysts are usually associated with the middle or lower thirds of the esophagus. Duplications of the small intestine may also be present.
A tract may extend between the enteric malformation and the adjacent vertebrae, and the enteric malformation often is adherent to the vertebral column. The tract may extend between the two halves of a cleft vertebra and even into the spinal canal; associated intraspinal neurenteric cysts may be present. In rare cases, the spinal cord and vertebral columns are split widely apart, forming 2 “neuraxial columns” between which lies a central cleft containing a variable amount of enteric tissue ranging from an enteric cyst to entire loops of bowel that pass through the midline cleft and lie posteriorly on the back of the child; this malformation is referred to as the “split notochord syndrome” or combined (anterior and posterior) spina bifida (Fig. 76-16). Associated intra-abdominal enteric duplications may also be present; in the extreme, complete hindgut duplication occurs with twinned colons extending from the level of Meckel diverticulum caudally, including double anuses. Girls additionally may have 2 vaginas, bilateral unicornuate uteri, and 2 bladders, each having a single ureter and urethra, which ends in its own urethral opening. Some girls have a bifid clitoris, and boys have a bifid penis. The spinal column also is doubled, with an associated split spinal cord.
Combined spina bifida (split notochord syndrome). A. Photograph of infant shows a huge, covered dorsal mass. B. Lateral x-ray shows multiple loops of bowel within the sec. (From Saunders RL. Combined anterior and posterior spina bifida in a living neonatal human female. Anat Rec 1976;87:255–278.)
The embryogenesis of SCMs and other complex dysraphic malformations is disputed, and several theories have been advanced. Beardmore and Wigglesworth proposed that before or during the outgrowth of the notochordal process, an adhesion could develop between the epiblast and hypoblast. This “endodermal–ectodermal adhesion” would provide a barrier to the elongating notochord, which would then become split around the adhesion; independent development of paired neuroepithelial anlagen would then form 2 “hemicords.” Associated remnants of the adhesion could give rise to endodermal remnants located anywhere between the gut and cutaneous ectoderm.
Noting the similarities between the central cleft in the split notochord syndrome and the neurenteric canal of normal embryos, both of which connect the amnion with the yolk sac, Bremer, proposed that these malformations must arise through the formation of an “accessory neurenteric canal” caused by a dorsal herniation of endoderm that splits the notochord and neuroepithelium. McLetchie and Saunders suggested that the initial malformation involves duplication of the notochord, which secondarily allows a endodermal–ectodermal interaction between the duplicated notochords.
Dias and Walker proposed that these and related complex dysraphic malformations arise during a time when prospective anlagen from all three germ layers are in intimate association, while they are being laid down during gastrulation. According to this theory, the notochordal and spinal cord precursors during gastrulation remain separate rather than integrating to form a single midline neuraxis and develop independently over a variable portion of their length to produce vertebral abnormalities and 2 “hemicords.” The intervening space between the paired “hemicords,” being comprised of pluripotent primitive streak cells, could form tissues derived from one or more of the three primary germ layers, including enteric structures (neurenteric cysts, intestinal duplications or diverticula, or loops of bowel within the central cleft), mesenchymal tissues (bony spurs or fibrous midline bands, blood vessels, muscle, and fat encountered between the 2 hemicords; anomalous vertebrae; and immature renal and Müllerian tissues), ectodermal tissues (dermal sinus tracts and/or dermoids), and even pathologic tissues such as teratomas and Wilms tumors.
Clinically, cutaneous stigmata of the underlying malformation are present in up to 80% of patients with SCMs. The most common (20% to 55% of patients) and specific of these is a focal area of hypertrichosis. Other cutaneous stigmata include cutaneous hemangiomata, dimples, lipomas, and bony abnormalities. Symptoms of spinal cord tethering occur because the 2 hemicords are transfixed by the intervening bony, cartilaginous, or fibrous tissues between the two hemicords. Sensorimotor deficits, changes in bowel or bladder habits, and orthopaedic deformities result. A “suspended” sensorimotor deficit (in which neurologic deficits are referable only to the involved spinal cord segments without more distal deficits) may arise presumably from local traction at the level of the malformation.
Radiographic evaluation of SCMs includes an MRI and/or a spinal CT scan with intrathecal contrast (a CT myelogram). Although the sensitivity of spinal MRI is improving, CT myelography is better to evaluate the fine details of these malformations for surgical planning. High-resolution CT myelography is particularly good at identifying thin intradural fibrous tethering bands in the type II malformations that may not be visible on MRI. About 15% of SCMs involve tandem lesions, so the entire spinal cord should be studied.
Prophylactic repair of the malformation and untethering are recommended by most before the child develops signs and symptoms because neurologic deficits, once they develop, are usually stabilized but may not improve with surgery. At surgery, the tethering bony spurs (type I) or fibrous bands (type II) are resected, and, in the type I malformations, the dural cuff between the two hemicords is excised and a single dural sac is reconstituted (described as “converting pants to a dress”). Any associated tethering elements should be dealt with as well. In particular, the filum terminale is almost always short and thickened and should be sectioned. Any associated enteric tracts should also be dealt with by the pediatric surgeon, usually following or concurrent with the neurosurgical repair.
Thickened Filum Terminale
The filum terminale is a nonfunctional strand of tissue that projects from the end of the conus to the bottom of the thecal sac and is formed from secondary neurulation. A thickened filum terminale is defined as one that is greater than 2-mm thick on MRI scans or CT myelography. The embryogenesis is unknown but likely involves a disturbance of the caudal cell mass during early embryogenesis. Up to 90% of malformations have fat within the filum terminale (the so-called “fatty filum”), and 86% are associated with a low-lying conus medullaris. Although as many as 6% of normal individuals have some fat within the filum, the association of a thickened, fat-infiltrated filum and a low-lying conus suggests a tethering lesion. As many as 50% of patients have cutaneous manifestations of the anomaly but in many, the initial presentation is with sensorimotor findings or a neurogenic bladder.
Plain x-rays sometimes demonstrate a defect in one or more vertebral laminae (spina bifida occulta). Spinal MRI demonstrates the low-lying spinal cord and a filum terminale that is thickened and infiltrated with fat (producing a hyperintense strand of tissue connecting the conus and the distal thecal sac on T1-weighted images). Surgical treatment involves a limited incision, sacral laminectomy, and simple section of the filum terminale near the end of the thecal sac.
A myelocystocele is a rare caudal spinal cord malformation in which there is dilation (terminal syringomyelia) of the caudal end of the spinal cord, with a corresponding dilatation of the caudal thecal sac, giving a “double bubble” appearance (Fig. 76-17) to the distal neuraxis on MRI. There is also usually an associated terminal spinal lipoma. The size of the malformation is variable, but some can reach a monstrous size (Fig. 76-17). The embryogenesis is unknown but again probably involves a disorder of caudal cell mass development. Clinically, the lesions appear as closed, skin-covered lumbosacral masses that resemble a spinal lipoma or sacrococcygeal teratoma. Many of these have erroneously been termed “closed myelomeningoceles” (a misnomer because, as previously discussed, a myelomeningocele cannot, be closed). Surgical treatment involves excising the redundant and nonfunctional dilated neural tissue, imbricating the remaining spinal cord, untethering the cord from the lipoma, and closing the thecal sac.
Myelocystocele. A. Photograph of an infant with cloacal exstrophy (repaired) and a huge skin-covered dorsal mass. B. Sagittal T1-weighted MRI shows a double compartment sac containing a dilated terminal spinal cord contained within a larger spinal fluid containing dural sac. (Photograph courtesy of Keith Aronyk, MD.)
The syndrome of caudal agenesis is usually included in the spectrum of dysraphic malformations, although tethering or other neurosurgical lesions are less frequent in these patients. The coccyx and part or all of the sacrum are usually missing. The agenesis rarely extends rostrally to involve the lumbar or even lower thoracic segments. The syndrome is more common in the offsprings of diabetic mothers (1% of the offsprings born to diabetic mothers will have sacral agenesis, and 16% of children with sacral agenesis are offsprings of diabetic mothers); both hyperglycemia and ketones have been implicated in the embryopathy. The embryonic mechanism is unknown, but a disorder of a caudal “embryonic field” has been implicated.
Clinically, the child with sacral agenesis has varying degrees of paralysis and atrophy of the distal leg musculature, producing an “inverted champagne bottle” appearance. The buttocks are flattened and atrophic as well. A neurogenic bladder is almost universal. Sensory function is curiously preserved. Lumbosacral spine x-rays reveal absence of a variable portion of the caudal spinal column, most commonly including part or all of the sacrum; hemivertebrae or fused vertebrae may also be seen. All children with sacral agenesis should undergo a baseline lumbosacral MRI to exclude important associated spinal cord malformations. The spinal cord ends bluntly within the thecal sac (Fig. 76-18), confirming the failure of caudal spinal cord development. Although sacral agenesis is a static malformation that need not be treated, associated tethering lesions (myelomeningoceles, SCMs, lipomas, dermoid tumors, fibrous bands, and thickened filum terminale) can all cause neurologic deterioration in these patients and should be treated if found. In addition, bony or dural stenosis of the spinal canal may cause progressive deterioration and may also require treatment.
Sagittal T1-weighted weighted MRI in a child with sacral agenesis shows absence of the bony sacrum and a blunted caudal spinal cord (curved arrow).
The Association of Imperforate Anus, Cloacal Exstrophy, OEIS, VACTERL, and Currarino Triad With Congenital Spinal Cord Malformations
The juxtaposition of the caudal neural tube (the conus medullaris below the second sacral spinal cord segment and the filum terminale) and the caudal spinal mesenchyme from the caudal cell mass, along with the hindgut endoderm and caudal urogenital system from the prospective cloaca during early development, results in the association between congenital anomalies involving cloacal derivatives and spinal cord malformations. Bony malformations of the sacrum (including agenesis, dysplasia, and/or asymmetry) are present in 30% to 38% of children with imperforate anus, including 48% of those with high imperforate anus; and 15% of those with low imperforate anus; genitourinary malformations are present in 20%. Associated congenital spinal cord anomalies are present in 10% to 14% of children with imperforate anus. Although more frequent in children with high imperforate anus, congenital spinal cord malformations also occur in children with low imperforate anus. Thickened filum terminale, spinal lipoma, and myelocystocele most commonly occur in association with anorectal malformations; less common anomalies include anterior meningoceles, syringomyelia, and dural stenosis. Caudal spinal cord anomalies also occur in association with the VACTERL (vertebral anomalies, imperforate anus, cardiac defects, tracheoesophagal fistula, renal anomalies, and limb reduction anomalies).
Caudal spinal cord malformations occur with even greater frequency in patients with cloacal exstrophy, where the spinal cord anomalies tend to be more complex than in those with isolated imperforate anus. Spinal cord malformations can also be seen as part of the OEIS (omphalocele, exstrophy, imperforate anus, and spinal defects) sequence, with 4 of 6 cases described by Carey as having skin-covered “meningoceles.” Among 13 patients with cloacal exstrophy and caudal spinal cord malformations described by Warf, 5 had myelocystoceles, 4 had spinal lipomas, and 3 had a thickened filum terminale.
The diagnostic evaluation for every patient with imperforate anus, anorectal stenosis, or cloacal exstrophy, regardless of the type, should include a spinal imaging study such as an MRI. Unfortunately, the associated problems with genitourinary and defecatory functions in this group of patients makes a proper clinical evaluation difficult; serial urodynamic studies are valuable for detecting occult urologic changes. In addition, particular attention should be given to the presence of associated neurologic deficits. Children with congenital tethering lesions should be offered neurosurgical repair and prophylactic untethering before symptoms and signs intervene.
Currarino triad is a distinct malformation sequence consisting of anorectal stenosis, a presacral mass, and an anterior sacral bony defect. The most common enteric malformations include anal or anorectal stenosis, although anorectal agenesis, anorectal stenosis with rectovaginal fistula, and rectal ectopia have also been described. An associated hemisacral or “scimitar” sacral defect (Fig. 76-19) is present; segmentation anomalies are less frequent. The presacral mass is most frequently a presacral teratoma or anterior meningocele; neurenteric cysts, or dermoid tumors are unusual. At least 50% of cases are familial, and both X-linked and autosomal dominant inheritance patterns have been described.
Unusual case of the Currarino triad. A. Anterior–posterior lumbosacral x-ray shows a scimitar defect in the bony sacrum. B. T2-weighted MRI shows a presacral teratoma (white arrows) and a low-lying spinal cord. At surgery, the spinal cord was split caudally, with one of the hemicords extending through the sacral defect to become contiguous with the presacral teratoma. (From Dias MS, Azizkhan RG. A novel embryogenetic mechanism for Currarino's triad: inadequate dorsoventral separation of the caudal eminence from hindgut endoderm. Pediatr Neurosurg 1998;28:223–229.)
This constellation of anomalies has been thought to arise through an abnormal adhesion or fistula between the neuroectoderm and endoderm in a manner analogous to the split-notochord syndrome, SCMs, and other complex dysraphic malformations described above. However, these embryonic mechanisms do not adequately fit our current understanding of caudal axial development because, unlike split-cord variants that involve more rostral regions of the neuroectoderm formed from primary neurulation, the Currarino triad involves neuroectoderm and caudal endodermal structures that are normally formed from the caudal cell mass. We encountered a child with the Currarino triad and a type II caudal SCM in which one hemicord was contiguous, through the sacral defect, with a presacral teratoma and an enteric duplication. This association of a caudal SCM with Currarino triad recently led us to propose that the Currarino triad arises through an incomplete dorsoventral separation of the caudal cell mass from the hindgut endoderm during late gastrulation.
Children with the Currarino triad most often present with constipation of varying degrees. Perirectal abscesses and fistula and meningitis are less common. Neurologic evaluation should include plain lumbosacral spine x-rays, which will demonstrate the scimitar sacrum to good advantage, and a lumbosacral MRI to evaluate the spinal cord and caudal neuraxial structures. A meningocele is most easily repaired via a posterior approach, ligating the opening of the thecal sac into the meningocele to seal it from the abdominal contents. Any tethering spinal cord elements should be dealt with before neurologic deficits intervene. Presacral teratomas should be treated as any sacrococcygeal teratoma.
In summary, congenital malformations of the central nervous system present a number of opportunities for interaction between the pediatric neurosurgeon and pediatric surgeon. We have emphasized the developmental anatomy of congenital malformations in this chapter because a thorough understanding of this anatomy helps one to best understand the intimate associations, as well as the borderland, between the central nervous system and other organ systems.