congenital brain and spinal cord malformations and their ... · the brain, spinal cord, and skin...

CLINICAL REPORT Guidance for the Clinician in Rendering Pediatric Care

Congenital Brain and Spinal CordMalformations and Their AssociatedCutaneous MarkersMark Dias, MD, FAANS, FAAP, Michael Partington, MD, FAANS, FAAP, the SECTION ON NEUROLOGIC SURGERY

abstractThe brain, spinal cord, and skin are all derived from the embryonic ectoderm;this common derivation leads to a high association between central nervoussystem dysraphic malformations and abnormalities of the overlying skin. Amyelomeningocele is an obvious open malformation, the identification of whichis not usually difficult. However, the relationship between congenital spinalcord malformations and other cutaneous malformations, such as dimples,vascular anomalies (including infantile hemangiomata and other vascularmalformations), congenital pigmented nevi or other hamartomata, or midlinehairy patches may be less obvious but no less important. Pediatricians shouldbe aware of these associations, recognize the cutaneous markers associatedwith congenital central nervous system malformations, and refer children withsuch markers to the appropriate specialist in a timely fashion for furtherevaluation and treatment.

INTRODUCTION

All pediatric care providers, regardless of specialty, encounter childrenwith manifestations of an underlying congenital, or dysraphic, brain orspinal cord malformation. Identifying and treating these dysraphic centralnervous system (CNS) malformations is important to prevent subsequentneurologic deterioration from spinal cord tethering, bacterial or chemicalmeningitis, or compression from growing mass lesions. The commonembryonic derivation of CNS and skin from ectoderm creates anassociation between CNS malformations and certain cutaneous markersthat, when recognized, affords an opportunity to identify andprophylactically treat the underlying CNS malformation. The purpose ofthis clinical report was to provide pediatric care providers with anoverview of these CNS malformations and their cutaneous manifestations,discussing (1) the early embryology of the CNS as it relates to theembryogenesis of these malformations; (2) the pathophysiology ofneurologic deterioration from spinal cord tethering; (3) a description ofcommon dysraphic malformations; (4) the relationship between

This document is copyrighted and is property of the AmericanAcademy of Pediatrics and its Board of Directors. All authors have filedconflict of interest statements with the American Academy ofPediatrics. Any conflicts have been resolved through a processapproved by the Board of Directors. The American Academy ofPediatrics has neither solicited nor accepted any commercialinvolvement in the development of the content of this publication.

Clinical reports from the American Academy of Pediatrics benefit fromexpertise and resources of liaisons and internal (AAP) and externalreviewers. However, clinical reports from the American Academy ofPediatrics may not reflect the views of the liaisons or theorganizations or government agencies that they represent.

The guidance in this report does not indicate an exclusive course oftreatment or serve as a standard of medical care. Variations, takinginto account individual circumstances, may be appropriate.

All clinical reports from the American Academy of Pediatricsautomatically expire 5 years after publication unless reaffirmed,revised, or retired at or before that time.

www.pediatrics.org/cgi/doi/10.1542/peds.2015-2854

DOI: 10.1542/peds.2015-2854

Accepted for publication Jul 30, 2015

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2015 by the American Academy of Pediatrics

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cutaneous markers and dysraphicmalformations; and (5) therelationship between other relatedmalformation sequences anddysraphism.

NORMAL EMBRYOLOGY AND THEPATHOPHYSIOLOGY OF SPINAL CORDTETHERING

Dysraphic CNS malformations ariseduring the second, third, and fourthweeks of human embryogenesis,generally referred to as the period ofneurulation. The neuroectoderm isfirst visible during the second weekas a pseudostratified columnarepithelium attached to the cutaneousectoderm around its periphery(Fig 1). During primary neurulation,the neuroepithelium elevates abouta midline central furrow; the 2 sides(the neural folds) then converge andfuse, forming a closed neural tube.The adjacent cutaneous ectodermseparates from the neuroectoderm(called dysjunction) to form theoverlying skin. The last sites to closeare the anterior neuropore at the levelof the future lamina terminalis(located just above the optic chiasm)and the posterior neuropore located atthe second sacral spinal cordsegment (S2). Dysraphicmalformations involving the brainand spinal cord down to the S2segment arise from disorderedprimary neurulation. Primaryneurulation is complete by the end ofthe fourth week.

The spinal cord below S2 and thefilum terminale are formed fromsecondary neurulation, which beginslate in the fourth week and involvesthe formation and subsequentfusion of multiple tubules ofneuroepithelial cells from the caudalcell mass. Secondary neurulationunderlies a fully formed cutaneousectoderm (skin) so that disorders ofsecondary neurulation give rise to“closed” malformations. Because thecaudal cell mass also gives rise to thesacrococcygeal spine, hindgut, andurogenital systems, dysraphic

malformations often coexist withmalformations of these structures.

As they are generated, the spinal cordand surrounding spine are the samelength; however, beginning at thesixth embryonic week, the spinal cordgrows more slowly than thesurrounding vertebral column,making the conus medullaris (CM)appear to “ascend” relative to the

surrounding spinal column. Thisascent of the conos medullaris placesthe conus opposite progressivelyhigher vertebral levels so that, by2 months after birth, the CM ends mostcommonly opposite the disc spacebetween the first and second lumbarvertebrae (L1-L2 disc space),1–3 withthe lowest normal level (95%confidence limits) being opposite the

FIGURE 1Scanning electron microscopy of primary neurulation in chick embryos. A, The neural plate existsinitially as a midline layer of pseudostratified columnar epithelium. B, The neural groove develops inthe midline of the neuroectoderm and the neural folds begin to elevate. The cutaneous ectoderm isattached laterally to the neuroectoderm. C, The neural folds begin to converge toward each other. D,The neural folds have fused and the cutaneous ectoderm has separated to form a layer of intact skinoverlying the neural tube. Reproduced with permission from Gilbert SF. Developmental Biology. 7th ed.Sunderland, MA: Sinauer Associates; 2003:394.

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middle third of the L2 vertebra.4 ACM that ends below the middle thirdof L2 is radiographically tethered,although whether this leads to theclinical features of the tethered cordsyndrome (see next paragraphs)requires clinical correlation.

Most dysraphic malformations likelyresult from disordered primary orsecondary neurulation. For example,myelomeningocele (MMC) representsa localized failure of primaryneurulation that results in an openneural tube that is still attachedperipherally to the adjacent skin(cutaneous ectoderm); an MMC istherefore, by definition, an openmalformation leaving the neural tubeexposed on the back. Dermal sinustracts (DSTs) may arise because offailed dysjunction in which a tongueof skin remains attached to the neuraltube. All dysraphic malformations,having in common a persistentanatomic connection between theneuroectoderm and cutaneousectoderm, have the inherent potentialto prevent proper ascent of the CMand cause “spinal cord tethering.” Thetethered cord syndrome refers toclinical deterioration resulting fromspinal cord tethering and has beenshown to involve physical stretchingof the spinal cord leading to impairedblood flow, diminished oxidativemetabolism and glucose utilization,and metabolic failure at the level ofthe mitochondrial respiratory chain.5

The severity and reversibility of thesemetabolic disturbances correlateswith the severity and chronicity of thetethering.

CLINICAL MANIFESTATIONS OF SPINALCORD TETHERING

The clinical signs and symptoms ofspinal cord tethering are somewhatage dependent. Infants are commonlyasymptomatic and the malformationsmay be recognized solely by theirassociated cutaneous abnormalitiesdiscussed later in this article.Symptoms in older children mayinclude pain, sensorimotor

disturbances of the lower limbs, anddifficulties with bladder and/orbowel control. Long-standinguntreated tethering can ultimatelyresult in progressive musculoskeletaldeformities and/or scoliosis.

As the child ages, muscle weaknessand gait disturbances may develop. Apreviously ambulatory child mayregress, may experience runningbecoming more difficult, and mightnot keep up with other childrenduring athletic activities. Muscleatrophy may become apparent, withthinning of calf muscles and/or“saber shins” that may bemisdiagnosed as Charcot-Marie-Toothsyndrome. Orthopedic deformities ofthe feet and spine deformities, suchas progressive scoliosis andexaggerated lumbosacral lordosis,may develop. As the child becomesmore verbal, back and/or leg painbecome a more common complaint.The pain varies and may be dull andaching; sharp, lancinating, orelectrical; or dysesthetic in character.The pain may be aggravated byflexion and extension of the spine orby walking or running. Pain in olderteenagers and adults may radiate intothe groin, genitals, and/or perianalregion.6 Objective sensory deficitsmay become more apparent as formaltesting becomes more reliable.Sensory abnormalities generally startdistally in the leg and become moreproximal over time; on occasion,a “suspended” sensory loss may bepresent with preserved sensationboth above and below the area ofabnormality. Difficulties with boweland bladder function may becomeevident with urinary and fecalurgency and/or incontinence, urinarytract infections, dribbling urinarystream, incomplete emptying, orinability to void.

People who become symptomatic asteenagers or adults often havea history of subtle abnormalitiesdating back to early childhood.6 Theymay always have been “slow”athletically, had difficulties with

chronic constipation or were late intoilet training, had previouslyrepaired orthopedic deformities orleg length discrepancies, or hadscoliosis. With long-standingtethering, the skin of the leg and footbecomes thin, shiny, and hairlessbecause of autonomic changes andlack of trophic influences; areas ofskin breakdown and chronicdiscoloration may appear as a resultof poor innervation, sensory loss, andrepeated unrecognized microtrauma.A characteristic feature of tetheredcord syndrome in adults is thesudden appearance of new pain and/or neurologic deficits after a suddenback stretching, such as duringchildbirth, falls onto the buttocks,vigorous sporting activities, andautomobile crashes.6

OVERVIEW OF SPINAL DYSRAPHICMALFORMATIONS

MMC

An MMC is the most common of thedysraphic malformations and is alsothe most serious CNS malformationcompatible with life. MMCs are thearchetype of the neural tube defectand represent a localized failure ofprimary neurulation. The resultantmalformation contains a placode ofneural tissue attached peripherallyto the surrounding skin (cutaneousectoderm) as it was in its embryonicstate (Fig 2). The underlyingcerebrospinal fluid (CSF) elevates theplacode on a dome or sac; if thethin tissue on the dome tears, the CSFis allowed to escape and themalformation is flat. Whetherdomed or flat, there will always bea placode on the skin surface and,by definition, MMCs are, therefore,open malformations.

The incidence of MMC has beendeclining over the past severaldecades, in large measure because ofpericonceptional folatesupplementation,7 with a currentbirth prevalence in the United Statesof approximately 0.2 per 1000 live

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births.8 The prevalence of neural tubedefects in the United States varies byethnicity, being highest amongHispanic infants at 1.12 per 1000 livebirths, lowest among AfricanAmerican and Asian infants at 0.75per 1000 live births, and intermediateamong non-Hispanic white infants at0.96 per 1000 live births.9 Theincidence of MMC also variesworldwide; for example, theincidence among continentalEuropean countries varies between 1in 1700 to 10 000 live births, whereasthe incidence in the British Islesvaries from 1 in 260 to 400. Irelandhas the highest rate in Europe, at 1 in200 live births.10 MMCs vary inappearance, size, and location;neurologic impairment generally isrelated to a larger size and morecranial location. Other associatedmalformations include hydrocephalusin 70%, Chiari type II malformation in98%, syringomyelia in 40% to 80%,and spinal cord tethering in virtuallyall. It is not the intent of this report toprovide details about all of theneurosurgical aspects of MMCs, asthere are many excellent reviews ofthis topic, including an article inPediatrics in Review.11

The rare cervical or high thoracicMMC (also referred to by some asa cervical myelocystocele because ofits ballooned-out dorsal fluidcollection) is a pedunculated, full-thickness, skin-covered, fluid-filledsac (usually having thinned,violaceous skin at its apex) located onthe neck or upper back of an infant(Fig 3A) and containing a small band

of tissue (Fig 3B) composed ofmesenchyme as well as both centraland peripheral neural tissue thatextends through a small defect in theposterior fascia and dura andattaches to the dorsum of the spinalcord. In contrast to the child with thetypical thoracolumbar orlumbosacral MMC who hassensorimotor paralysis correspondingto the level of the malformation,children with cervical meningoceleshave few if any neurologicdeficits.12,13 It is vital to understandthis point so that parents can beproperly counseled if this condition isdiagnosed prenatally.

Meningocele

A meningocele (Fig 4) is an isolatedfull skin thickness sac, filled with CSFand lacking central nervous issue. Onmagnetic resonance imaging (MRI),the meningocele sac contains onlyfluid without any visible tissue. Thefrequency of meningoceles is one-tenth that of MMCs. Affected childrengenerally have no neurologic deficits.Meningoceles have been thought notto contain tethering elements, butcareful dissection may disclosea fibrous tract that connects the innerlining of the sac with the spinal cord;a meningocele can, therefore, causetethering.

Atretic Meningocele

An atretic spinal meningocele is raremalformation consisting of a small,flat area of dysplastic skin that lookslike and has been referred to as“scarified,” “cigarette paper,” ora “cigarette burn”14 (Fig 5). The lesionis flat or slightly indented, sometimespainful to touch, and sometimessurrounded by a cuff ofhyperpigmented skin (Fig 5A) ora cutaneous salmon-colored capillarymalformation (Fig 5B). There isusually an underlying fibrous tissuetract (also called a meningocelemanqué) that, like the fibrous tract ofthe meningocele described in theprevious section (and the DSTdescribed subsequently), passes

through the fascia, posterior vertebralelements, and dura, and attaches tothe dorsum of the spinal cord.14

Lipomyelomeningocele/Myelocystocele/Enlarged or FattyFilum Terminale

Lipomyelomeningocele,myelocystocele, and enlarged and/orfat-infiltrated filum terminale all havein common some element of fatwithin the spinal cord and/or filumterminale; they may representdifferent manifestations of the sameembryogenetic process and are,therefore, discussed together. Alipomyelomeningocele (also calleda spinal lipoma) is a malformation inwhich a fatty subcutaneous massextends into the vertebral canal andends as an intramedullary spinal cordmass. Most spinal lipomas havea visible fatty mass, sometimeswith an associated capillarymalformation, infantile hemangioma,and/or dimple (Fig 6). However,a minority have no associated skinmanifestations.Lipomyelomeningoceles may bedorsal (arising from the dorsum ofthe spinal cord), terminal (arisingfrom the filum terminale or the tip of

FIGURE 2MMC. The placode can be seen with its midlineneural groove and is attached to the skinaround its edges.

FIGURE 3Cervical MMC. A, Lateral view showing full-thickness skin with violaceous apex and nocerebrospinal fluid leakage. B, Operative viewdemonstrating the thin stalk of tissue arisingfrom a small fascial defect.


the CM), or transitional (arising fromthe junction of the 2 and having bothdorsal and terminal components).15

In a fourth subtype, the spinal cordactually exits the spinal canal distallywithin the fatty mass.16 The fat withinthe lipomyelomeningocele is readilyidentified as a hyperintense mass onT1-weighted MRI sequences; caudallesions may contain additional tissuetypes and appear heterogeneous onMRI.

Myelocystoceles most commonlypresent as full-thickness, skin-covered lumbosacral masses (Fig 7)that sometimes are referred toerroneously as “closed MMCs.” Amyelocystocele has 3 componentsthat are visible on MRI scans: (1)a dilated terminal spinal cordcontained within (2) an even morelargely dilated distal dural sac(commonly described on MRI asa “sac within a sac”), and (3) anadjacent spinal cord lipoma.17,18

Children with myelocystocele may benormal or have variable neurologic

deficits depending on the size andseverity of the malformation.

Fatty filum terminale (also called anenlarged or thickened filum) is anenlarged filum (defined as .2 mm incross-sectional diameter on MRIscans) that is often (although notinvariably) infiltrated with fat; assuch, some consider the thickenedfatty filum terminale to be a formefruste of terminal lipoma.

All 3 of these conditions may arisealone or in association with caudalmalformations involving other organsystems, such as anorectalmalformations, cloacal exstrophy,VACTERL (vertebral defects, analatresia, cardiac defects, tracheo-esophageal fistula, renal anomalies,and limb abnormalities), OEIScomplex (omphalocele, exstrophy,imperforate anus, spinal cordtethering), and other disorders of thecaudal cell mass.

Split Cord Malformation

A split cord malformation (SCM) isa malformation in which the spinalcord splits over a portion of its lengthinto 2 separate “hemicords” with anintervening, tissue-containing cleft.Two types have been described.19

Type I contains 2 hemicords, eachcontained with its own separate duralsac (analogous to 2 legs within 2 pantlegs) and having an interveningextradural bony or cartilaginoustethering spike. Type II (previously

referred to as diplomyelia) contains 2hemicords within a single dural sac(analogous to 2 legs within a singlepant leg) and usually having a fibrousband of tissue connected to thesurrounding dura. A thickened and/or foreshortened filum terminaleserves as an additional tetheringelement. The most commoncutaneous manifestation of an SCM isa fawn’s tail or hairy patch on theback (Fig 8); other less commoncutaneous manifestations includecapillary malformations, DSTs, orsubcutaneous masses.

SCMs can occur in isolation or may beassociated with a variety of othercongenital malformations, includingMMC, lipomyelomeningocele, DSTs,neurenteric cysts, cervicothoracicmyelocystoceles, sacral agenesis, andsome cases of Klippel-Feil syndrome.Vertebral malformations arecommon, especially in SCM type I,and most commonly includehemivertebrae, sagittally clefted(butterfly) vertebrae, or fused (block)vertebrae. Visceral malformationsmay include enteric duplications,fistulae, or malrotations; neurentericcysts; missing or ectopic kidneys; andother malformations.20

Lumbosacral DSTs and InnocentCoccygeal Dimples

A spinal DST is a midline congenitalepithelial-lined tract that can ariseanywhere along the spine but mostcommonly occurs at S2 (representingthe posterior neuropore as themost complex region of caudalneural tube closure).21 DSTs arethought to arise embryologicallythrough incomplete dysjunction,leaving a tongue of cutaneousectoderm attached to theneuroectoderm during primaryneural tube closure. Spinal DSTsoccur with a frequency of ∼1 in 2500live births.21 A skin dimple ispresent on the flat portion of thesacrum well above the upper end ofthe gluteal cleft.21 The dimple has anunderlying tract of epithelial andfibrous tissue that pierces the

FIGURE 4Meningocele, covered with full-thickness skin.

FIGURE 5Atretic meningocele. A, Scarified “cigarette paper” skin lesion. B, Similar lesion with surroundingcapillary malformation.


underlying fascia and posteriorvertebral elements, pierces the dura,and tracks cranially within thesubarachnoid space to end on thedorsal aspect of the CM.

It is important to distinguish thelumbosacral DST from the innocentcoccygeal dimple or pit, an innocentfinding in ∼4% of the population.22

Generations of physicians have beentaught that a dimple is innocent ifits base can be visualized andabnormal if its bottom cannot beseen; this teaching is incorrect. Thepresence or absence of a “bottom” tothe dimple has little to do with itspathologic nature. Rather, it is thelocation of the dimple along thecraniocaudal axis that is the mostimportant feature. As the nameimplies, the innocent coccygealdimple is more caudally located thanthe pathologic lumbosacral DST. It

most commonly lies withina centimeter of the coccyx within thegluteal cleft and usually is invisibleunless the buttocks cheeks are parted(Fig 9); a finger placed over thedimple can usually be rolled over thetip of the underlying coccyx. A goodrule of thumb is that if one draws animaginary line between the tops ofthe 2 forks of the gluteal cleft,a dimple at or below this line isnormal, whereas a dimple locatedabove this line is abnormal. Coccygealdimples have no associated skinabnormalities and are not associatedwith any signs or symptoms oftethering. They are not, nor do theygive rise to, pilonidal sinuses,dimples, or cysts. Imaging ofcoccygeal dimples is not necessary22;the tract extends from the pit to thecoccygeal tip, well below the end ofthe thecal sac, and is not connected tothe spinal cord (Fig 9). Isolatedcoccygeal dimples do not requirefurther workup or treatment.

In contrast, the DST is lumbosacral,located cranial to the gluteal cleft onthe flat part of the sacrum (Fig 10A).DSTs are sometimes associated withsurrounding cutaneousmanifestations, such as vascularanomalies (Fig 10B), tufts of hair(Fig 10C), skin tags, or subcutaneousdermoid masses (Fig 10D). Thesetracts are always abnormal andrequire surgical correction. SpinalDSTs present clinically in 1 of 5 ways:(1) the presence of a cutaneous tract;(2) a CNS infection, such asmeningitis or intraspinal abscess; (3)aseptic meningitis resulting fromdesquamation of epithelial cells froman associated dermoid or epidermoidcyst; (4) spinal cord compressionfrom the growth of an intra- orextradural dermoid or epidermoidcyst; and (5) neurologic deteriorationfrom tethering. Infection is the mostfeared complication, both because itcan be highly morbid and because itgenerates an intradural scar thatmakes excision of the tract muchmore difficult without creatingadditional neurologic deficits.

FIGURE 6Spinal lipoma. A, Subcutaneous mass with overlying faint pink capillary malformation (NFS or“salmon patch”). B, An otherwise invisible spinal lipoma associated with an overlying pink NFS withindistinct borders. C, An otherwise invisible spinal lipoma associated with an overlying raised sacralinfantile hemangioma having distinct borders. D, A PWS.

FIGURE 7Large myelocystocele.


Spinal DSTs may be investigatedusing spinal ultrasonography and/orMRI, although it is important to pointout that the decision to treat is madesolely on the presence of thepathologic dimple, regardless ofimaging findings. The DST may not bevisualized, and the spinal cord is notalways radiographically tethered(ie, below the mid-body of L2); evenhigh-resolution MRI may miss asmany as 50% of DSTs.21 The value ofneuroimaging is, therefore, largely tolook for associated anomalies or thepresence of dermoid or epidermoidcyst(s) as part of surgical planning.

All spinal DSTs should be repairedregardless of imaging studies,because prophylactic treatment

minimizes the risks of subsequentcomplications. The tract is completelyexcised down to its attachment to thespinal cord, because removing onlythe superficial subcutaneous portionof the tract does not eliminatetethering, aseptic meningitis, orgrowth of dermoid/epidermoid cysts.

Currarino Triad

Currarino triad is a very rare caudalmalformation that combines ananorectal malformation (anorectalstenosis or agenesis, anorectalstenosis with rectovaginal fistula, oranal ectopia), a sacral bony defect(usually hemisacral agenesis with“scimitar sacrum”), and a presacralmass (most commonly a presacralteratoma or anterior sacralmeningocele, less commonlya neurenteric or dermoid cyst).23–25 Agenetic linkage can be established in50% of cases with autosomaldominant and recessive as well asX-linked forms having beendescribed26–28; multiple geneticmutations involving the HLXB9homeobox gene have beendescribed.29 The embryonicmechanism appears to involve anabnormality of dorsoventralpatterning within the caudal cellmass.29,30 Associated dysraphicmalformations are uncommon.30 Thepresacral malformation may presentas an enlarging pelvic mass duringchildhood or escape detection duringchildhood and present in adults,sometimes during pregnancy whenthe meningocele ruptures duringdelivery and causes meningitis.

Caudal Agenesis (Including Sacraland Lumbosacral Agenesis)

Caudal agenesis is a disorder in whichthe caudalmost portions of the spineand spinal cord do not developproperly (dysgenesis) or at all(agenesis). Most commonly, thesacrum (the second sacral segmentand below) and coccyx are absent(sacral agenesis), although rarely thecondition extends to the lumbar spineas well (lumbosacral agenesis).

Additionally, the correspondingsegments of the spinal cord areabsent, producing a characteristicblunted CM on MRI scans.31 The filumterminale is also invariably absentin complete sacral agenesis, althoughit may be present (and tether thespinal cord) in sacral dysgenesis.Maternal gestational diabetes isa well-described risk factor for sacralagenesis. Sacral agenesis may occurin isolation or in association withother caudal malformations, such asanorectal malformations, cloacal orbladder exstrophy, VACTERL, OEIS,and other disorders of the caudal cellmass.31 Bony sacral dysgenesis alsocan occur in isolation or asa component of the Currarino triad,discussed previously, as a “scimitarsacrum.”

Children with sacral agenesis havecharacteristically flattened buttockswith a shallow gluteal cleft,a palpably absent coccyx, and distalleg wasting described as an “invertedchampagne bottle” appearance(Fig 11). Distal leg and foot weaknessare common, although sensation iscuriously spared. Bowel and bladderdysfunction are universal. Althoughmost children with sacral agenesishave fixed and static neurologicdeficits, a minority can manifestprogressive neurologic deteriorationas a result of either to dural orbony spinal stenosis or, more rarely,spinal cord tethering from anassociated thickened filum terminaleor another congenital spinal cordmalformation.32

OVERVIEW OF CRANIAL DYSRAPHICMALFORMATIONS

Anencephaly

Anencephaly is the cranial analog ofMMC resulting from failure ofanterior neural tube closure. Themalformation is obvious at birth;open, exposed, and undifferentiatedneural tissue is present above theorbital rims and nuchal line.Anencephaly is virtually always fatal

FIGURE 8Fawn tail in child with split cord malformation.

FIGURE 9Benign coccygeal dimple within the gluteal cleftand overlying the tip of the coccyx.


during infancy; neurologic outcome inthe few identified survivors is poor.No treatment is available.

Cranial DSTs

Cranial DSTs are less common thanspinal DSTs. Like spinal DSTs, cranialDSTs can produce symptoms by (1)serving as a portal of entry forbacteria and producing meningitis,subdural empyema, or brain abscess;(2) causing aseptic meningitisthrough the desquamation ofepithelial debris from the tract and/or associated dermoid or epidermoidcysts; and (3) causing intracranialhypertension and/or focal braincompression through the progressiveenlargement of an intracranial

dermoid or epidermoid cyst. CranialDSTs are recognized as midline pitsor dimples located between theglabella and nasal tip33 (Fig 12A) orin the parieto-occipital region(Fig 13A) but are not found betweenthese areas. Although subcutaneousdermoid and epidermoid cysts mayarise at the anterior fontanelle, theydo not extend intracranially.

Frontonasal DSTs are innocuousappearing and could easily beoverlooked or misdiagnosed aspimples or comedones. Sebaceous orcreamy fluid can sometimes beexpressed from the ostium; clear CSFmay drain on rare occasions. Asubcutaneous tract extends to theskull base between the nasal bone

and nasal cartilage.33 An associateddermoid or epidermoid cyst ora small heterotopic mass of astrocytesand even neurons (called a nasalglioma) may be present within thetract. Although 70% to 90% of thesetracts end extracranially, 10% to 30%extend to a variable extentintracranially through the skull baseat the foramen cecum (Fig 12B).33,34

Computed tomography (CT) and MRIprovide complementary informationin the detection of frontonasal DSTs.CT may reveal bony defects withinthe foramen cecum or intracranialcalcifications, whereas MRI maydetect the soft tissue components ofthe tract and/or intracranial dermoidor epidermoid cysts.35 Unfortunately,intracranial tracts may not always bevisible. Treating frontonasal DSTsregardless of the imaging findingseliminates the tract and preventsfuture complications, even thoughmost will involve only a local nasalexcision.

Parieto-occipital DSTs morefrequently have intracranial extensionthrough a midline occipital skulldefect, penetrate the dura, and endintracranially in relation to either theoccipital lobes or posterior fossa;associated dermoid cysts may bepresent (Fig 13B). Although MRI ismost useful to identify intracranialextension, CT again may playa supplementary role in identifying

FIGURE 11Inverted champagne bottle appearance of legswith sacral agenesis.

FIGURE 10Lumbosacral DSTs. A, DST superiorly (arrow) with deviated gluteal cleft inferiorly. B, DST withsurrounding infantile hemangioma. C, DST with skin appendage and hair in ostium. D, Subcutaneousdermoid.


small bony ostia through which thetract might extend.

Encephaloceles

Encephaloceles represent focalherniation of meninges, with orwithout brain tissue, througha focal defect in the skull and arethought by many to arise afterneurulation from a defect in thecalvarial mesenchyme rather than asa neural tube defect. They may beisolated malformations or associated

with a wide variety of other geneticsyndromes and malformationsequences.36 Encephaloceles mayinvolve the calvarium or skull base.Calvarial encephaloceles can ariseanywhere along the midline skullfrom the orbits to the craniocervicaljunction. Occipital encephalocelesare most common in European andNorth American populations, whereasfrontal encephaloceles are mostcommon among Asian populations.Calvarial encephaloceles are readily

apparent externally as fully skin-covered sacs containing variableamounts of CSF and/or brain. Frontalencephaloceles may have associatedhypertelorism. Tissue may extendinto the orbits or the frontal, ethmoid,and sphenoid sinuses, where theymay cause proptosis or present asintranasal or pharyngeal masses(neuroimaging should, therefore, beconsidered before surgical biopsy ofan intranasal mass). Encephalocelesmay rarely extend through defects inthe sphenoid or petrous bones intothe pterygopalatine or infratemporalfossae and may be completelyinvisible externally.

Neuroimaging defines both the extentand type of neural tissue within thesac. MRI provides superiorvisualization and is the preferredimaging modality. The outcome forencephaloceles is variable anddepends, in large measure, on theamount and type of neural tissuewithin the sac. For example, largeoccipital encephaloceles containingsolely or largely CSF may have anexcellent prognosis, whereas thosehaving large amounts of occipital lobeor brainstem generally have a poorprognosis.

The atretic parieto-occipitalencephalocele deserves specialmention, because it can be confusedwith cutis aplasia congenita (CAC)(described later). Midline atreticencephaloceles overly the parietal oroccipital bones as a small area ofdysplastic skin surrounded by whorlsof distinctly colored hair sometimesreferred to as a “horse collar”(Fig 14A). Neuroimaging maydemonstrate an underlying smallbony defect and/or a bifid superiorsagittal sinus. In addition, MRI, andparticularly magnetic resonancevenography, may show a classicvenous drainage pattern in which thestraight sinus is atretic or absentand the deep cerebral veins insteaddrain through an embryonic primitiveprosencephalic (or falcine) veinbetween the pineal region and

FIGURE 12Frontonasal DST. A, DST arising from the glabella. B, Sagittal T2-weighted MRI showing dermoid cyst(arrow) with tract extending through the anterior skull base at the level of the foramen cecum(arrowhead).

FIGURE 13Occipital DST. A, Midline tract. B, Sagittal T1-weighted MRI showing DST (arrow) with large posteriorfossa dermoid tumor (asterisk).


superior sagittal sinus37 (Fig 14B). Atsurgery, the atretic parieto-occipitalencephalocele contains an underlyingtissue tract having a surroundingdural cuff. Despite its innocuousappearance, the parietalencephalocele may be associatedwith other congenital brainmalformations and significantcognitive deficits in some cases.38,39

Parietal encephaloceles must bedistinguished from CAC, a disorder offull-thickness skin of uncertainetiology that most commonly involvesthe scalp (Fig 15); 20% to 30%have skull aplasia as well.40 In themidline, CAC may extend to involvethe dura.41 Both genetic transmission(autosomal dominant and, lesscommonly, autosomal recessive) andassociation with chromosomalabnormalities (trisomy 13, deletion ofthe short arm of chromosome 4) havebeen described.40 Unlike the skin-covered atretic encephalocele,CAC lacks skin and does notcharacteristically have a dysplasticskin collar or a whorl of surrounding

hair; it has no intracranial tract oftissue and is associated with neitherany underlying brain malformationnor intracranial venous anomalies. ACAC can, nonetheless, be dangerousfor 2 reasons: first, it can serve asa portal of entry for bacterialmeningitis or intracranial infection.Second, if allowed to desiccate fromexposure to air, the dura lining thesuperior sagittal sinus can crack andbleed significantly. A midline CAC thatexposes the superior sagittal sinusshould be immediately covered witha sterile, saline-soaked gauze orpetroleum gel until repaired bya neurosurgeon and/or plasticsurgeon.

RELEVANCE OF CUTANEOUS MARKERS

Cutaneous markers may be the onlyindication of an underlying spinalcord malformation, particularly ininfants before progressive symptomsor neurologic deficits develop. Facedwith a child having a cutaneousmarker, the pediatrician is facedwith a decision to (1) observe; (2)obtain some sort of imaging studyand, if so, what type; and/or (3)obtain a neurosurgical consultation.Unfortunately, there are fewprospective studies that meaningfullyassess the frequency of underlyingspinal cord malformations for thesecutaneous markers, and thepredictive value of these markers isimplied largely from older studies onthe natural history or surgicaloutcomes of occult dysraphism.However, cutaneous anomalies maygenerally be stratified into 3 risk

categories based on the literature andcollective experience (Table 1).

High-Risk Cutaneous Anomalies

Children with 1 or more of thecutaneous markers described in thefollowing paragraphs often have anunderlying congenital spinal cordmalformation. Almost 70% ofchildren with congenital spinal cordmalformations display at least 1 ofthese high-risk cutaneousmarkers,42,43 and it is common for 2or more cutaneous markers tocoexist. On the other hand, thesehigh-risk cutaneous markers arepresent in only 3% of normalneonates.44

Hypertrichosis refers to a focal tuft ofhair of variable thickness located inthe posterior spinal midline (Fig 8C);because it resembles a horse’s tail,it has earned the mythologicalname “fawn’s tail.”43 This can bedistinguished by its focality from themore diffuse and/or “light hair” oftenseen in infants (discussed in thesection Low-Risk CutaneousAnomalies, later in this article).Hypertrichosis is often accompaniedby a capillary hemangioma and alsomay be associated with dimples orsubcutaneous masses, such as lipoma,bone malformations, or eventeratoma. Hypertrichosis mayaccompany spinal malformations ofany type but is most commonlyassociated with split cordmalformations, where it is associatedwith two-thirds of type I andone-third of type II SCMs.19,43

An infantile hemangioma (Fig 6C) isa highly vascular, usually raised lesionhaving well-defined borders. It isreadily distinguished from the flatport wine, pink, or salmon-coloredcapillary malformations discussed inthe next section, Intermediate-RiskCutaneous Anomalies. Infantilehemangiomas develop in up to 5% ofinfants and may be located anywhereon the body. Infantile hemangiomasthat are midline and overlie the spine,particularly in the lumbar region, are

FIGURE 14Atretic parietal encephaloceles. A, Scarifiedmidline lesion with whorl of surrounding hair(or “horse collar”). B, Magnetic resonancevenogram showing persistent falcine vein(arrowheads) and absence of straight sinus(arrow).

FIGURE 15CAC.


sometimes associated withunderlying dysraphicmalformations.45 Although thesensitivity and specificity of thelumbosacral midline infantilehemangioma as a marker for spinaldysraphism are not entirely known,the presence of this marker raisessuspicion for an underlying dysraphicmalformation.43,45,46 A subset ofinfantile hemangiomas overlying thelumbosacral spine that are segmental,are large, and may have a reticularpattern are associated with spinal andgenital urinary malformations in upto 55% of cases as part of theLUMBAR syndrome (lower bodyhemangioma and other cutaneousdefects, urogenital abnormalities,ulcerations, myelopathy, bony defects,anorectal malformations, arterialanomalies, and renal anomalies).47

Caudal appendages represent focalskin-covered appendages describedas true tails and pseudotails48

(Fig 16). A true tail is a vestige of theembryonic tail that ordinarilyregresses in humans; it containsvertebrae and variably muscle, fat,and mesenchymal tissues. The tailmay be covered with hair and is oftencapable of spontaneous or reflexmovements.48 In contrast,a pseudotail is a skin-coveredoutgrowth containing fat, cartilage, orother organ-specific tissues, such asembryonic kidney. It is thought to bean abnormal outgrowth rather thana vestigial embryonic structure. Thisdifferentiation is moot from

a practical standpoint, because bothtrue tails and pseudotails may beassociated with dysraphicmalformations (although somestudies suggest a more frequentassociation with pseudotails).

Atretic meningocele (Fig 5) is anotherhigh-risk cutaneous marker that wasdiscussed previously.

Intermediate-Risk CutaneousAnomalies

Capillary vascular malformations maybe classified as intermediate-riskanomalies and are of several types; allare flat malformations in contrast tomost infantile hemangiomas, andmicroscopically they look similardespite the differences in theirclinical appearance. Port wine stains(PWSs) are flat, darker, red-purplelesions, having well-defined borders,which tend to get darker with time(Fig 6D). Nevus flammeus simplex(NFS),49 also referred to as “salmonpatch,” is a flat, pink or red capillarymalformation having relatively ill-defined borders. These lesions arepresent in up to 43% of the generalpopulation49,50 and occur in a varietyof locations. Nonmidline lesions aswell as midline lesions that occur onthe glabella, the lip (“angel kiss”) orthe nape of the neck (“stork bite”) arenot associated with underlyingdysraphic malformations. On theother hand, midline or juxta-midlinelumbosacral lesions are sometimesseen in association with dysraphicmalformations including DSTs, split

cord malformations,lipomyelomeningoceles (Fig 6A, 6B),and other malformations.

Whether isolated midline lumbosacralcapillary malformations, particularlyNFS, which are present in as many as0.77% of the healthy population,49

are more frequently associated withunderlying dysraphic malformationsis controversial. In one study of 120children with spinal dysraphicmalformations, a capillarymalformation was the only cutaneousmanifestation of the underlying spinalcord abnormality in 17%.51 On theother hand, 2 studies involvinga combined 40 infants with capillaryvascular malformations but no othercutaneous markers of dysraphismidentified only 1 (2.5%) with anunderlying dysraphic malformationon spinal ultrasonography.49 IsolatedNFS is much less frequentlyassociated with dysraphicmalformations than are PWSs.However, NFS may not always be easyto distinguish from PWSs clinically,leading to confusion and impreciseterminology.

Low-Risk Cutaneous Anomalies

A number of low-risk cutaneousmarkers do not require routinefurther neuroimaging or follow-up.

TABLE 1 Risk Stratification for Various Cutaneous Markers

High Risk Intermediate Risk Low Risk

Hypertrichosis Capillary malformations (alsoreferred to as NFS or salmonpatch when pink and poorlydefined, or PWS when darker redand well defined)

Coccygeal dimpleInfantile hemangioma Light hairAtretic meningocele Isolated café au laít spotsDST Mongolian spotsSubcutaneous lipoma Hypo- and hypermelanotic

macules or papulesCaudal appendage Deviated or forked gluteal

cleftSegmental hemangiomas in

association with LUMBARsyndrome

Nonmidline lesions

LUMBAR, lower body hemangioma and other cutaneous defects, urogenital abnormalities, ulcerations, myelopathy, bonydefects, anorectal malformations, arterial anomalies, and renal anomalies.

FIGURE 16Pseudotail.


These include non-midline cutaneouslesions, benign coccygeal dimples(discussed previously); diffuse andevenly distributed lumbosacral hair,isolated café au laít and Mongolianspots, hypo- and hypermelanoticmacules or papules, and isolatedgluteal cleft deviation or forking.There have been no large prospectivestudies of isolated gluteal cleftabnormalities. One studydemonstrated that isolated glutealcleft deviation or forking carriesa low association with dysraphicmalformations,52 although a higherincidence is found when gluteal cleftabnormalities are combined withother cutaneous markers ofdysraphism. Absent other cutaneousmarkers of dysraphism, isolatedgluteal cleft abnormalities need not befurther evaluated, but those that occurwith other cutaneous markers ofdysraphism and those havingneurologic, urologic, or orthopedicmanifestations of tethering suggest anunderlying dysraphic malformation.

ASSOCIATED CONDITIONS

Scoliosis, Orthopedic Deformities,and Dysraphism

As many as 75% or more of patientswith spinal dysraphism will presentwith lower extremity neurologic andorthopedic abnormalities fromtethering.53 The exact presentationdepends on both the age of thepatient and the degree and type oflower extremity dysfunction.53–55

Progression is an important featurethat suggests an underlying dysraphicmalformation with spinal cordtethering. Unfortunately, althoughtethered cord release is effective inarresting or improving neurologicsymptoms, sensorimotor dysfunction,or urologic deterioration, long-standing or severe orthopedicdeformities are unlikely to improve,and subsequent orthopedicintervention may be required.

Scoliosis is another commonmanifestation of tethering.56 Like

other orthopedic manifestations,scoliosis associated with tethering isoften progressive and may bea levoscoliosis rather than the morecommon dextroscoliosis seen inidiopathic scoliosis in some,57,58 butnot all59 studies. Scoliosis in thesetting of dysraphism is multifactorialand may involve muscular imbalance,vertebral abnormalities, and otherfactors; for example, 18% to 58% ofdysraphic malformations areassociated vertebral malformations,such as hemivertebrae, butterflyvertebrae, or segmentationabnormalities,60,61 and it may bedifficult in this setting to determinewhat role, if any, tethering plays in thedevelopment of scoliosis. However,scoliosis that is atypical, rapidlyprogressive (in excess of the rate ofannual progression predicted by theassociated vertebral malformations),or associated with neurologicabnormalities should prompt furtherworkup and referral. Fortunately,early untethering can often haltprogression and may even reversedeformities and restore function,particularly for those with maturespines and/or scoliosis curves of,40 degrees.55,56,60,62–65

Anorectal Malformations andDysraphism

The intimate temporospatialrelationships between caudal spinalcord and anorectal and urogenitaldevelopment during earlyembryogenesis may result inassociated malformations involvingall 3 organ systems.66 Between 10%and 52% of children with anorectalmalformations have associateddysraphic malformations.67–73

Studies have not establisheda correlation with the level of theanorectal malformation (low,intermediate, or high),74,75 althoughthere is a higher association withcomplex (43%) compared withsimple anorectal malformations(11%). Both dysraphic and anorectalmalformations may occur inconjunction with recognized

malformation sequences such asCurrarino triad, VACTERL, and OEIS.MRI will identify children havingunderlying dysraphic malformations.

Urologic Dysfunction andDysraphism

Urologic dysfunction is an importantpresenting feature of spinal cordtethering.76,77 Urologic function maybe assessed by history (incontinence,frequency, repeated urinary tractinfections), imaging (renalultrasonography showinghydroureter/hydronephrosis,sometimes with associated small,enlarged, or trabeculated bladder) orby formal urodynamic testing inwhich the bladder’s response toretrograde filling is assessed.78,79

Urologic manifestations of tetheredcord vary according to the age atpresentation and the severity of theresponse to the tetheringprocess.80,81 More than 90% ofchildren younger than 3 years atdiagnosis have no urologic symptoms,and results of formal urodynamictesting at this age are rarelyabnormal.78,82 Urinary tract infectionis the predominant sign in an affectedinfant, but urinary retention isoccasionally seen.77 Once a child istoilet trained, the onset of secondaryurinary incontinence, especially inconjunction with fecal incontinenceand/or constipation, is the mostcommon presentation of a tetheringlesion, although urinary tractinfection is still common in this agegroup as well.77,81,83 As the childmatures, urgency, urge incontinence,sudden or stress incontinence, new-onset enuresis, urinary frequency,and nocturia, often together withfecal soiling, are the most commonmodes of presentation. Renalultrasonography may revealhydronephrosis and/or increasedbladder wall thickness. In addition,a plain abdominal radiograph mayreveal bony abnormalities of thespine or disturbances in the bowelgas pattern. Urodynamic studies atthis time demonstrate either an


enlarged bladder capacity withdetrusor underactivity (no or poorbladder contractions) and denervationin the external urethral sphinctermuscle (signs of lower motor neurondysfunction) or a small, thick-walledbladder with detrusor overactivity andincoordination between the bladderand external sphincter muscle withvoiding, called detrusor sphincterdyssynergia (signs of upper motorneuron dysfunction).79,82

Urologic and/or gastrointestinalsymptoms in a child with a cutaneousmidline skin lesion or with leg pain,sensorimotor loss, orthopedicdeformity, or gait disturbancesuggests an underlying spinal cordtethering malformation. A trainedpediatric urologist will be able toidentify and characterize voidingdysfunction in this population.84,85

A urodynamic evaluation beforesurgical correction providesinformation about the extent ofsacral spinal cord involvement andserves as a basis for comparisonpostoperatively.78,86

SUMMARY AND CONCLUSIONS

A wide variety of congenital brain andspinal cord malformations mayultimately lead to neurologicdeterioration. Cutaneousmanifestations of dysraphicmalformations are common, and theirpresence may alert the pediatric careprovider to the presence of anunderlying spinal cord abnormality,especially in association witha pattern of other signs andsymptoms that suggest spinal cordtethering. Recognizing andprophylactically treating thesemalformations often provides thebest opportunity to avoidsubsequent deterioration.

LEAD AUTHORS

Mark S. Dias, MD, FAANS, FAAPMichael Partington, MD, FAANS, FAAP

CONTRIBUTING AUTHORS

Stuart B. Bauer, MD, FAAPRobin Bowman, MD, FAANS, FAAP

Bermans Iskandar, MD, FAANS, FAAPMarc A. Levitt, MD, FAAPDavid G. McLone, MD, FAANSFrancesco T. Mangano, DO, FACS, FACOJerry Oakes, MD, FAANS, FAAPJohn Sarwark, MD, FAAPElizabeth Tyler-Kabara, MD, FAANS, FAAPShokei Yamada, MD, FAANS, FAAP

SECTION ON NEUROLOGIC SURGERYEXECUTIVE COMMITTEE, 2015-2016

John Ragheb, MD, FAAPPhillip R. Aldana, MD, FAAPAnn-Christine Duhaime, MD, FAAPAndrew H. Jea, MD, FAAPDouglas Brockmeyer, MD, FAAPAnn Ritter, MD, FAAP

FORMER SECTION ON NEUROLOGICALSURGERY EXECUTIVE COMMITTEEMEMBERS

Mark S. Dias, MD, FAANS, FAAP, ImmediatePast ChairDavid P. Gruber, MD, FAAP

STAFF

Vivian ThorneLynn Colegrove, MBA

ABBREVIATIONS

CAC: cutis aplasia congenitaCM: conus medullarisCNS: central nervous systemCSF: cerebrospinal fluidCT: computed tomographyDST: dermal sinus tractMMC: myelomeningoceleMRI: magnetic resonance imagingNFS: nevus flammeus simplexOEIS complex: omphalocele,

exstrophy,imperforate anus,spinal cordtethering

PWS: port wine stainSCM: split cord malformationVACTERL: vertebral defects, anal

atresia, cardiac defects,tracheo-esophagealfistula, renal anomalies,and limb abnormalities

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