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J Neurosurg (6 Suppl Pediatrics) 103:512–523, 2005

Neurenteric cysts in children: 16 consecutive cases and review of the literature RICARDO SANTOS DE OLIVEIRA, M.D., GIUSEPPE CINALLI, M.D., THOMAS ROUJEAU, M.D., CHRISTIAN SAINTE-ROSE, M.D., ALAIN PIERRE-KAHN, M.D., AND MICHEL ZERAH, M.D. Division of Neurosurgery, Hospital of Clinics of Ribeirão Preto, São Paulo, Brazil; Department of Neurosurgery, Santobono-Pausilipon Children’s Hospital, Naples, Italy; and Department of Neurosurgery, L’Hôpital Necker–Enfants Malades, Assistance Publique, Hopitaux de Paris, Université Paris V, Paris, France Object. The authors of this retrospective review and analysis of the literature cover an institutional series of neurenteric cysts of the central nervous system in children treated in the magnetic resonance imaging era during a 14-year period. Methods. Sixteen patients 20 days to 14 years of age are described. The most frequent signs and symptoms at presentation were acute spinal cord compression (11 patients), paresis of a cranial nerve (two patients), meningitis or infection (two patients), and intracranial hypertension (one patient). The locations of the cysts were as follows: in the spinal canal in 12 patients (75%), the clivus in two (12.5%), the cavernous sinus in one (6%), and the craniocervical junction in one (6%). The most common location was the ventral aspect of the spinal canal (seven patients). Associated spinal deformities were found in five patients. All patients underwent surgery, with a posterior approach used in all of the spinal cases. Total resection was achieved in 12 of the 16 cases and partial resection in four. Of the four patients who underwent subtotal resection, the cyst recurred in three, requiring further surgery. Conclusions. Neurenteric cysts are uncommon congenital anomalies that can present acutely in the pediatric population. Total removal is usually possible and is associated with a good prognosis.

KEY WORDS • neurenteric cyst • split notochord syndrome • spinal dysraphism • enterogenous cyst • spinal cyst • pediatric neurosurgery

N

EURENTERIC or enterogenous cysts are uncommon congenital lesions that result from displaced elements of the alimentary canal and are commonly encountered in the posterior mediastinum. These cysts can occur (albeit rarely) at any level of the neuraxis from the posterior clinoid to the coccyx; they are most commonly found in the lower cervical and upper thoracic regions.1,8, 84,96 The lesions are generally located ventral to the spinal cord and cervicomedullary junction.1,74 The mesodermal disturbance is often reflected by the presence of associated VB anomalies.21,88 The cysts consist of mucin-producing, nonciliated epithelium that is simple or pseudostratified and either cuboidal or columnar.111,122 The patients may present neurologically with signs of spinal cord compression and meningitis,11 but the clinical symptoms associated with neurenteric cysts depend on the site of the lesion.36,89 We describe a series of 16 children who presented consecutively and review the literature.

Abbreviations used in this paper: CNS = central nervous system; CSF = cerebrospinal fluid; MR = magnetic resonance; VB = vertebral body.

512

Clinical Material and Methods Sixteen patients with neurenteric cysts underwent surgery consecutively between 1986 and 2000. All patients were seen in our department at the time of the diagnosis. The nine male and seven female patients ranged from 20 days to 14 years of age (mean age 3.8 years; median 4 years). The diagnosis was confirmed histologically in all cases. Each patient’s age at the time of diagnosis, sex, and presenting symptoms as well as the anatomical location of the cysts are displayed in Table 1. Magnetic resonance imaging was undertaken in all patients. Surgical Procedure

All patients were treated surgically; in 11 cases surgery was performed in an emergency situation. All of the spinal cases were initially approached via the posterior route. Three cases needed a second approach (posterior and transoral). The cyst contents were waterlike in seven cases and had a whitish, viscous material in nine. In our series, a posterior approach through laminoplasty was chosen as a first surgery in all of the spinal cases. After opening of the dura mater, the lesion can usually be seen on J. Neurosurg: Pediatrics / Volume 103 / December, 2005

11 yrs, M 5 yrs, F

2 3

3rd cranial nerve palsy

J. Neurosurg: Pediatrics / Volume 103 / December, 2005

4 yrs, M 6 yrs, F 2 yrs, F

7 yrs, M

3 wks, M paraplegia 4 yrs, M paraparesis 40 wks, M occult dysraphism 4 wks, F paraparesis

9 10 11

12

13 14 15

paraparesis

acute

acute chronic chronic

acute

acute chronic acute

acute

chronic

acute acute

chronic

acute acute

acute

Symptom Onset

L5–S1

none none

none

Cutaneous Stigmata

Klippel–Feil/scoliosis; none vertebral hemifusion none none none none

none none

none

Bone Abnormality

prespinal cord

prespinal cord intramedullary prespinal cord

none none subcutaneous mass none

intradural, dorsal spina bifida (subcutaneous mass)

dorsal meningocele

spina bifida/scoliosis; vertebral hemifusion none none none none diastematomyelia hairy patch

none none diastematomyelia

intra/extradural spina bifida; enlarged cutaneous hecervical spinal canal mangioma intramedullary intramedullary none none

prespinal cord prespinal cord

prespinal cord

clivus clivus

cranial

Cyst Position

T-10, intradural intramedullary T12–L1, intradural prespinal cord prespinal cord L2–3, intradural

T7–9, intradural

C4–7, intramedullary C5–T3, intradural C7–T1, intradural C7–T1, intradural

C3–5

C1–4, intradural C2–4, intradural

craniocervical

clivus clivus

cavernous sinus

Cyst Location Level

partial

total total total

total

total total total

total

partial

total total

partial

total total

partial

Type of Resection

* FU = follow-up; NA = not applicable; pst = posterior. † Transitory diabetes insipidus. ‡ Initial diagnosis was retropharyngeal abscess; the patient underwent surgery four times before the neurenteric cyst was removed. § The child experienced hypertensive hydrocephalus and a shunt was inserted. || Cervical deformation 4 months after surgery that required anterior cervical fixation. ** Transitory postoperative leakage of CSF.

16

tetraparesis

6 yrs, M

8

tetraparesis sensitivity issues paraparesis

tetraparesis

5 wks, F

7

5 6

4

2 yrs, F

1

Neurological Finding

visual deficit retropharyngeal abscess 1 yr, F recurrent meningitis 20 days, M tetraparesis 14 yrs, M tetraparesis

Age at Op, Sex

Case No.

Initial Op Approach

intact

improved improved||

intact§

intact† intact‡

meningocele ex- intact** cision

pst laminoplasty died pst laminectomy intact pst laminoplasty intact

pst laminoplasty intact

pst laminoplasty intact pst laminoplasty intact pst laminoplasty improved

pst laminoplasty intact

pst fossa craniotomy pst laminoplasty posterolat route & laminoplasty pst laminoplasty

transoral route transoral route

yes

no no no

no

no no no

yes

no

no no

yes

no no

yes

Neurological RecurOutcome rence

craniotomy & intact cyst aspiration

TABLE 1 Clinical characteristics and outcome in 16 patients with neurenteric cysts*

pst laminoplasty

NA NA NA

NA

NA NA NA

clinical

NA

transoral route NA NA

craniotomy & cyst resection NA NA

Procedure

1.5

20 days 11.0 2.0

6.0

2.5 14.0 8.0

8.0

10.0

4.0 5.0

3.0

1.0 4.0

3.0

FU (yrs)

Neurenteric cysts in children

513

R. S. de Oliveira, et al. the side of the spinal cord. After sectioning the dentate ligament on the side in which the cyst is more visible (although they are usually strictly midline lesions, some asymmetry in the posterior expansion is typically observed), the lesion is gently punctured with a very small needle and the clear fluid content is aspirated slowly to avoid sudden decompression of the spinal cord. After partial aspiration and decompression of the cyst, its wall can be dissected very easily from the spinal roots and from the neural structures of the spinal canal. In many cases, the spinal cord is so thin that with subtle rotation movements its anterolateral surface can be controlled using adequate inclination of the microscope, allowing gentle dissection of the cyst wall—which is not very adherent in primary cases (that is, those without previous meningitis). In all of these cases, it was possible to remove the cyst totally or subtotally through gentle dissection and traction of the membrane, with no recurrence or clinical deterioration. We observed no tight adhesions of the lesion to the spinal cord in these patients. Patient Outcome

The follow-up period ranged from 20 days to 14 years (mean age of the patients 5 years, median age 4 years). The

postoperative neurological status was considered excellent in 12 of the 16 cases. Three patients had persistent neurological deficits: one with moderate kyphosis and spasticity in the right arm (Case 6), one with mild hemiparesis (Case 5), and one with scoliosis and weakness in the lower extremities (Case 11). A newborn (Case 13) presented with neonatal tetraplegia and died after surgery of respiratory complications. Results The most common signs and symptoms of neurenteric cysts were as follows: compression of the spinal cord in 12 patients (75%), paresis of a cranial nerve in two (12.5%), meningitis or infectious syndrome in two (12.5%), and intracranial hypertension in one (6%). Six patients presented with bone malformations (37.5%), four with cutaneous anomalies (dorsal meningocele, hairy patch, cutaneous hemangioma, and subcutaneous mass), and three with other malformations (clubfoot, rib and thorax anomalies, and abdominal anomalies). We observed an acute neurological deterioration in 11 patients (68.7%). The locations of the neurenteric cysts (Fig. 1) were as follows: in the spinal canal in 12 patients (75%), the clivus

FIG. 1. The topography of several neurenteric cysts as depicted on MR images. Upper Left: Case 4. Midsagittal T1weighted image of the craniocervical junction. Upper Right: Case 6. Midsagittal T1-weighted image of a cyst in the cervical prespinal cord. Lower Left: Case 1. Axial T1-weighted image of an intracavernomatous cyst. Lower Right: Case 10. Midsagittal T2-weighted image of an intramedullary cyst.

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Neurenteric cysts in children in two (12.5%), the cavernous sinus in one (6%), and the craniocervical junction in one (6%). The posterior cervical region was the most common location in the spinal canal in six patients (50%). Among the spinal cases, the cyst was located ventral to the spinal cord in seven patients (43.7%) and was intramedullary in three (18.7%), intra- and extradural as well as intramedullary in one (6.2%), and intradural and dorsal in one (6.2%). Associated spinal deformities (Klippel–Feil anomaly, diastematomyelia, scoliosis and vertebral hemifusion, spina bifida, and enlarged cervical spinal canal) were found in five patients. The appearances of the cysts on MR imaging are summarized in Table 2. We performed 22 operative procedures in 16 patients. Emergency surgical treatment was undertaken in 11 patients (68.7%). The posterior approach to the spinal canal was the most common route as a first procedure in 11 cases (68.7%), whereas the approach was transoral in two (12.5%), posterolateral in one (6%), combined in one (6%), and cranial in one (6%). Surgical complications were observed in three cases (18.7%; namely, cervical deformation, diabetes insipidus, and CSF leakage). Despite immobilization with a Minerva brace, the child (Case 6) in whom a cervical deformity had developed required anterior cervical fixation 4 months postoperatively (Table 1). Complete resection of the cyst was possible in 12 patients, but partial removal only was achieved in four (25%). Of the four patients who underwent subtotal resection, the cyst recurred in three, necessitating further surgery. The four recurrences were in Cases 1, 4, 8, and 16. Case 1 involved the cavernous sinus, and a simple aspiration was performed during the first surgery. The patient in Case 4 had had four occurrences of meningitis before the diagnosis; this was our only case with tight adhesions. Partial removal led to recurrence and repeated operation via a transoral route. A partial resection of the cyst was performed in Case 8; 2 years later we observed a recurrence of the lesion. This patient remained clinically stable, so no surgical approach was proposed. The patient in Case 16 underwent surgery on Day 2 of life with the preoperative misdiagnosis of a meningocele; partial removal led to a rapid recurrence, which was treated surgically at a later time. Discussion The first intraspinal endodermal cyst that was histologically verified was reported and termed “intestinoma”96 in 1934, but some authors14,59 described (in 1928 and 1934, respectively) a typical case of neurenteric cyst that they designated as a teratomatous cyst of the spinal cord. Since the description by Puusepp,96 the first account of a pediatric cyst of this nature verified histologically was published in 1937 in an autopsy case.58 We conducted a literature review of 121 neurosurgical pediatric cases that were verified histologically (with an upper limit of 18 years of age). Table 3 summarizes the cases of pediatric neurenteric cysts. Recently, in a clinicopathological study of 145 cysts of the CNS investigators identified five neurenteric cysts of the spine,113 and in a series of 15 neurenteric spinal cysts,98 eight pediatric cases were identified. There are some discrepancies in the literature regarding the classification of neurenteric cysts in relation to their embryological origin.27 It is generally accepted that they are J. Neurosurg: Pediatrics / Volume 103 / December, 2005

TABLE 2 Characteristics of the MR imaging signal in 16 patients with neurenteric cysts MRI Signal Case No.

T1-Weighted

T2-Weighted

Ring Contrast Enhancement

Cyst Content

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

hypointense isointense isointense hypointense hyperintense hypointense isointense hypointense hypointense mixed hypointense isointense hypointense mixed hypointense hypointense

hyperintense isointense isointense hyperintense hyperintense hyperintense hyperintense hyperintense hyperintense mixed hyperintense isointense hyperintense mixed hyperintense hyperintense

no yes no no no no yes no no no no no no no no no

waterlike waterlike waterlike viscous viscous viscous waterlike waterlike viscous viscous viscous waterlike viscous waterlike viscous viscous

components of the split notochord syndrome.74,106 These lesions are a form of spina bifida occulta typically consisting of an intradural cyst lined by mucin-producing nonciliated epithelium that is simple or pseudostratified (columnar or cuboidal). The cyst can be ciliated or it can have a mixture of gastrointestinal, pancreatic, and/or squamous epithelium.1,22,122 Some authors have analyzed scanning electron microscopy images of such cysts and described a possible relation to the respiratory tract.80 These cysts represent 0.3 to 0.5% of spinal tumors.39,113 In 1929, Feller and Sternberg31 reviewed a series of infants born with varying degrees of CNS and intestinal anomalies. They concluded that the neurenteric anomalies appeared after the development of the notochord and the neural tube from a group of cells issued from the Hansen node, and they defined a classification for these anomalies. In 1976, neurenteric cysts were reclassified into three types by Wilkins and Odom122 based on histological features. Type A cysts are lined by a single layer of pseudostratified cuboidal or columnar epithelial cells that mimic gastrointestinal or respiratory epithelium; they appear with or without cilia lining on a basement membrane and are supported by a layer of vascular connective tissue. Type B cysts, constituted by the epithelial lining, may be arranged in complex invaginations and contain glandular organization, usually producing mucin or serous fluid, smooth muscle, striated muscle, fat, cartilage, bone, elastic fibers, lymphoid tissue, nerve fibers, ganglion cells, or Vater–Pacini corpuscles. Type C cysts, the most complex, contain ependymal or glial tissue.38 Immunohistochemical studies have an important role in the diagnosis of these lesions.47 Defects in VBs and intraabdominal or intrathoracic cysts are frequently encountered in association with these cysts.64 Neurenteric cysts can be classified based on the relative positions in the spinal cord, vertebral column, and alimentary canal.8 This classification is applicable to the more severe forms of the anomaly. For anomalies of a lesser degree, the classification of Smith is more practical.112 This classification comes under the rubric 515

516

Lerma, et al., 1985 Matsushima, et al., 1985 Itakura, et al., 1986 Kantrowitz, et al., 1986

Takemi, et al., 1984 Chavda, et al., 1985

Arnould, et al., 1965 Dorsey & Tabrisky, 1966 Prop, et al., 1967 Brun & Saldeen, 1968 Kahn, et al., 1971 Klump, 1971 Deshpande, et al., 1972 Reddy, et al., 1972 Silvernail & Brown, 1972 Bale, 1973 Gardner, 1973 Kinoshita & Tokuda, 1973 Okino, et al., 1973 Yamashita, et al., 1973 Laha & Huestis, 1975 Voth, et al., 1975 Odake, et al., 1976 Evans & Lougheed, 1978 Holmes, et al., 1978 Ohwaki, et al., 1978 Guilburd, et al., 1980 Husson, et al., 1981 Carachi, 1982 Schiffer & Till, 1982 Woo & Sharr, 1982 Fortuna & Mercuri, 1983

Hoefnagel, et al., 1962 Voth, et al., 1963 Rewcastle & Francoeur, 1964

Knight, et al., 1955 Neuhauser, et al., 1958

Kubie & Fulton, 1928 Bucy & Haymond, 1932 Ingraham, 1938

Authors & Year

2 yrs, M 15 mos, F 10 wks, M 2 yrs, M 1 yr, M 4 yrs, M 4 yrs, M 6 yrs, F 24 wks, F 15 yrs, M 18 yrs, M 15 yrs, F 17 yrs, M 18 yrs, M 10 wks, F 2 days, M 6 yrs, F 8 wks, M 11 yrs, M 3 yrs, M 12 yrs, M 6 days, F 6 yrs, M 8 yrs, M 14 yrs, M 14 yrs, F 4 yrs, M 10 yrs, M 1 day, F 13 yrs, M 13 yrs, M 3 yrs, M 13 yrs, M 13 yrs, F 4 yrs, F 3 yrs, M 1 yr, M 18 yrs, M 18 yrs, F 12 yrs, F 10 yrs, F 18 yrs, M 8 yrs, M 13 yrs, M 7 yrs, F 6 yrs, F 3 yrs, M 8 yrs, F 4 yrs, F 1 yr, M

Age at Op, Sex

intradural, T10–12 intradural, lumbar intradural, C6–7 intradural, T9–11 intramedullary, T3–5 intradural, T3–4 intradural, C7–T1 intradural, C5–6 intradural, C7–T1 intradural, T12–L2 intradural, T11–L3 intradural, C5–6 intradural, L2–S4 intradural, C7–T1 intradural, lumbosacral intradural, thoracic intradural, C6–7 intradural, C5–T1 intramedullary, C1–3 intradural T6–9 intramedullary, T-2 intradural, T2–4 intradural C3–T1 intradural, C1–3 intradural, C7–T1 intramedullary, C6–7 intradural, C3–T1 intradural, T3–5 intramedullary, L5–S1 intradural, C1–3 intradural, T1–2 intradural, C3–4 intradural, L1–3 posterior fossa intramedullary, T9–10 intradural, C3–4 intradural, C-2 intradural, C4–5 intradural, C3–4 intramedullary, C3–5 intradural, C5–6 intradural, C5–7 intradural, T-2 intradural, T-2 intradural, T3–4 intradural, L1–2 intradural, C6–7 intradural, C5–T1 intradural, C1–2 intramedullary, C5–T8

Cyst Location

progressive paraparesis & back pain mass in lumbar region dermal sinus & fever back pain & irritability irritability & cervical rigidity chest mass & repeated respiratory infections scoliosis & lt-sided weakness progressive hemiplegia fever & cervical x-ray anomalies intermittent low-back pain progressive paraparesis progressive tetraparesis chronic sensory motor symptoms neck pain & hemisensitive symptoms lumbosacral mass myelomeningocele tetraparesis hemiparesis –– –– gradual hemiparesis diastematomyelia persistent fever & spastic paraparesis tetraplegia back pain & paraplegia progressive tetraparesis upper paraparesis & neck pain paraplegia meningomyelocele neck pain & tetraparesis upper paraparesis & neck pain –– low-back pain craniofacial pain & 3rd nerve palsy spastic paraparesis progressive tetraparesis hemiparesis & severe neck retraction spastic paraparesis tetraparesis neck pain & tetraparesis neck pain, torticolis, & paraparesis neck pain w/ upper-limb paraparesis back thoracic pain spastic paraparesis back pain & spasticity of both legs low-back pain spastic paraparesis spastic paraparesis –– fever & acute paraparesis


chronic chronic acute acute chronic chronic chronic chronic acute chronic chronic acute chronic chronic acute acute acute acute –– –– chronic acute chronic acute acute chronic chronic chronic acute acute chronic –– acute acute chronic acute acute chronic chronic acute chronic chronic acute chronic chronic chronic chronic chronic –– acute

Symptom Onset

TABLE 3 Cases of pediatric neurenteric cysts in the literature*

yes yes yes yes yes yes yes no yes no no no yes yes yes yes no no no yes yes yes yes no yes yes yes yes yes no no yes no no yes no no no no no yes yes no no no yes no no no yes

Vertebral Change

yes yes yes no yes yes yes yes yes yes yes no no no yes no yes yes –– –– no no yes no yes yes yes yes yes yes no –– yes no yes no yes no yes no yes yes no yes no yes no no –– yes

Total Removal

cured cured died recurred† cured cured –– cured cured cured cured improved improved recurred‡ improved death improved cured –– –– improved died§ improved cured improved cured cured|| improved improved cured cured –– cured recurred** improved cured improved improved cured cured cured cured recurred†† cured recurred‡‡ cured recurred§§ cured –– cured

Outcome

R. S. de Oliveira, et al.



Hamamoto, et al., 1997 Mochida, et al., 1997 Rebhandl, et al., 1998 Hassan, et al., 1999

Rao, et al., 1996 Sarkar, et al., 1996

Midha, et al., 1995 Lieb, et al., 1996 Mam, et al., 1996 Prasad, et al., 1996

Lazareff & Hoil Parra, 1995 Menezes & Ryken, 1995

LeDoux, et al., 1993 Pianetti Filho & Fonseca, 1993 Devkota, et al., 1994 Languepin, et al., 1994 Mendel, et al., 1994 Mooney, et al., 1994

Brooks, et al., 1993

Morita, et al., 1990 Turgutalp, et al., 1991 Arai, et al., 1992 Kemp & Towbin, 1992 Bollini, et al., 1993

Miyagi, et al., 1988 Mizuno, et al., 1988 Van der Wal & Troost, 1988 Ebisu, et al., 1990

Inoue, et al., 1988

Alrabeeah, et al., 1988

Velasco-Siles, et al., 1986

Authors & Year

2.5 yrs, M 7.5 yrs, M 9 yrs, M 4 wks, M 13 yrs, F 8 yrs, F 11 yrs, F 11 yrs, F 6 yrs, M 4 yrs, F 1 day, F 1 day, M 11 yrs, M 32 wks, M 16 yrs, M 32 wks, F 3 mos, F 12 wks, M 2 yrs, F 2 mos, F 6 yrs, F 22 wks, M 13 yrs, M 3 yrs, M 12 wks, M 12 yrs, F 6 yrs, M 2 wks, M 5 yrs, F 2 yrs, F 12 yrs, M 5 yrs, M 1.5 yrs, M 7 yrs, F 6 yrs, M 8 yrs, F 4 yrs, F 14 yrs, M 16 wks, F 10 yrs, M 11 yrs, M 6 yrs, M 18 yrs, M 16 yrs, F 16 yrs, M 2 mos, M 7 yrs, M 7 yrs, F 8 yrs, M 16 yrs, M

Age at Op, Sex

intradural, C7–T2 intradural, T3–7 intradural, C5–6 extra/intradural, C3–T1 extra/intradural, L5–S1 intradural, C5–T1 intradural, C-3 intradural, C3–5 intramedullary, C2–5 brainstem intramedullary, lumbar intramedullary, L5–S1 intradural, C3–7 intradural, lumbar intradural, C5–6 intradural, C2–6 intradural, S3–5 intramedullary, L3–S1 intradural, S1–3 intradural, S4–5 intramedullary, T6–7 intradural, T1–3 intradural, C1–2 intradural, T1–4 intradural, L1–S4 intradural, C1–3 intradural, C4–6 intradural, C1–3 intradural, lumbar extra/intradural, T4–6 extra/intradural, T3–4 extra/intradural, T4–8 extra/intradural, T4–5 intradural, C2–4 intradural, C2–4 intradural, C1–2 intradural, C5–6 intradural, C1–4 intradural, C1–2 intradural, T-4 intradural, C6–T1 intradural, C5–6 intradural, C2–3 extradural, T12–L1 intradural, L1–3 extra/intradural, T6–7 intramedullary, C4–6 intradural, C3–5 intradural, T1–2 intradural, L2–3

Cyst Location

spastic tetraparesis & neck pain spastic paraparesis rt hemiparesis & neck pain chest mass recurrent meningitis & pelvic infection spastic paraparesis tetraplegia progressive tetraparesis hemiparesis cranial nerve palsy meningomyelocele meningomyelocele bilat shoulder pain mass in lumbar region progressive paraparesis limited neck flexion & irritability meningitis & paraparesis lower-limb motor deficits meningitis, back pain, & lower-limb deficits lumbar cutaneous anomalies paraparesis spastic paraplegia upper-extremity paraparesis spastic tetraparesis meningitis tetraparesis & neck pain neck pain & paraparesis apnea & spastic tetraparesis paraparesis & spina bifida progressive kyphoscoliosis spastic paraparesis & kyphosis progressive paraparesis mild pectus carinatum neck pain & tetraparesis neck pain & tetraparesis recurrent meningitis tetraparesis paraparesis recurrent meningitis paraplegia neck pain & paraparesis spastic paraparesis pain & rt upper-limb weakness back pain back pain & lower-limb weakness dyspnea & lower-limb weakness tetraparesis persistent neck pain precordial pain low-back pain


chronic chronic chronic acute chronic chronic acute chronic acute chronic acute acute acute chronic chronic acute acute chronic acute chronic acute acute chronic acute acute chronic chronic acute chronic chronic chronic chronic chronic chronic chronic acute chronic acute chronic –– acute chronic chronic chronic chronic acute acute chronic chronic chronic

Symptom Onset

TABLE 3 Cases of pediatric neurenteric cysts in the literature (continued)

yes no no yes yes no no yes no no yes yes no yes no no yes yes no yes no yes yes yes yes no yes no yes yes yes yes yes yes no no yes no no yes yes yes no no no yes no no no no

Vertebral Change

yes yes yes yes yes no no no no yes yes yes no yes no yes yes yes yes yes yes yes yes yes yes yes yes yes yes no no yes no yes yes yes yes no no yes yes yes yes yes yes yes yes no no yes

Total Removal

improved|||| cured cured cured cured –– –– cureda recurredb improved improved improved recurrencec cured cured cured cured improved died cured cured –– cured cured cured cured cured improved improved died aggravated improvedd recurrede cured cured cured improved recurredf recurredg cured cured cured cured improved cured died cured cured cured cured

Outcome

Neurenteric cysts in children

517

518

4 yrs, F 2 yrs, M 3 yrs, M 5 yrs, F 3 yrs, M 8 wks, F 10 yrs, F 5 yrs, M 17 yrs, M 18 yrs, M 5 yrs, F 17 yrs, M 9 yrs, F 10 wks, M 4 yrs, M 8 yrs, M 1 yr, F 6 wks, F 5 wks, F 2 yrs, M 3 yrs, M

Age at Op, Sex

intradural, T12–L1 intradural, C3–5 extradural, T7–8 intradural, C4–T2 intradural, C3–4 extra/intradural, T6–9 intradural, C6–7 intramedullary, C3–5 intradural, L3–5 intradural, L5–S3 intradural, T3–7 intradural, T12–L3 intradural, C2–3 extra/intradural, T2–3 intradural, L1–3 intramedullary, L-5 intradural, T11–L2 intramedullary, T12–L1 intradural, L1–2 intradural, C7–T1 intramedullary, T1–7

Cyst Location

paraparesis tetraparesis paraparesis tetraparesis neck pain & tetraparesis paraparesis neck stiffness & ataxia fever, headaches, & neck stiffness paraparesis & back pain paraparesis progressive paraparesis pain & leg length discrepancy back pain & scoliosis posterior mediastinal mass back pain back & rt leg pain lumbar subcutaneous mass hairy patch lumbar mass paraplegia paraplegia


acute acute acute acute chronic acute chronic acute chronic chronic chronic chronic chronic acute chronic chronic acute chronic acute acute acute

Symptom Onset

yes no yes no no yes no no yes no yes yes yes yes yes yes yes yes yes no no

Vertebral Change

* –– = data not available. † Recurrence 8 years after operation. ‡ Recurrence of anterior cyst 1 year after first surgery. § This child underwent surgery at 12 days and the osseous spur was excised. The child died 10 days later. A diagnosis of neurenteric cyst was made at necropsy. || The child underwent surgery at the age of 3 weeks for a cystic mediastinal mass with no evidence of communication with spinal cord. ** Recurrence 2 years later (new partial surgery) & new recurrence 3 years after second surgery. †† Recurrence at 12 and 14 years of age. ‡‡ Recurrence at 18 years of age. §§ Recurrence 2 years later; patient underwent surgery. |||| Associated mediastinal mass removed by a right thoracotomy. a Initial syringomyelia was surgically treated 2 years before the neurenteric lesion was removed. b Recurrence of cyst 8 years after first surgery. c First surgery to treat cyst 8 years before recurrence. d Progressive kyphosis in later postoperative period; the child underwent posterior spinal fusion. e Progressive kyphosis 10 years later (posterior spinal fusion) and resection of recurrent neurenteric cyst. f Recurrence 1 year postoperatively. The clinical appearance of the patient was normal 3 months after second operation. g Recurrence 16 months after first surgery. h Recurrence at the age of 8 months and surgery was performed to treat the mediastinal mass at 18 months. i Recurrence after partial removal. j Recurrence 14 months after initial surgery.

Rizk, et al., 2001 Agrawal, et al., 2002

Rauzzino, et al., 2001

Kumar, et al., 2001

Ergun, et al., 2000 Kadhim, et al., 2000 Fan, et al., 2001

Kim, et al., 1999

Authors & Year

TABLE 3 Cases of pediatric neurenteric cysts in the literature (continued)

yes no no no yes no yes no yes yes yes no yes yes no yes yes yes yes yes no

Total Removal

improved improved improved improved cured recurredh cured recurredi improved improved improved recurredi cured cured recurred j cured cured cured cured cured improved

Outcome



Neurenteric cysts in children of split notochord syndrome35,95 because the concept seems basic to the mechanism underlying the communication between the entoderm and the dorsum of the embryo.81 The spectrum of anomalies according to Smith’s classification includes alimentary diverticula through prevertebral posterior enteric cysts to VB malformations with intraspinal cyst to posterior spina bifida and dermal sinus.35,62 Neurenteric cysts are most frequently found in the posterior mediastinum1,90,122 and can give rise to neurological defects.3,22,50,61,70,79,83,93,114 Superina and colleagues114 published a series that included cystic duplications of the esophagus and neurenteric cysts. The series consisted of a total of 15 chest masses and eight lesions of the CNS. They concluded that a spinal component may accompany the mediastinal cyst in as many as 20% of cases and they suggested a systematic radiological examination of the spinal canal in cases of chest masses. In one third of the patients, neurenteric cysts are associated with complex malformations of the CNS and/or gastrointestinal tract and can be detected on prenatal ultrasonography images.10,19,32,37,69,102 Durham and associates23 have demonstrated that neurenteric cysts can be associated with the Currarino Triad. Agnoli, et al.,1 observed that of 33 intraspinal cysts verified histologically, 18 were located in the cervicothoracic spine (80% were intradural extramedullary and 12% were intramedullary). In a review of the pediatric literature, these cysts have been found to be midline benign lesions that can occur at any level of the neuraxis. The most commonly found type and location was intradural in the spinal canal in 114 (94.2%) of 121 instances, followed by cervical (28%), thoracic (20.6%), cervicothoracic (11.5%), lumbar (8.2%), thoracolumbar (4.9%), lumbosacral (4.1%), and sacral (2.4%). The intramedullary form represented 14% of the cases and had a cervical and thoracic predominance.11,15,20,24, 30,40,52,57,77,84,98,111,115,125

The cysts have been found predominantly ventral to the spinal cord in the cervical and thoracic spinal subarachnoid space, with a lower incidence at the lumbar and sacral levels41,54,60,65,73,74,116 and the craniocervical junction.12,22,26,48,53,64,97 In one pediatric review, however, the cyst was found dorsal to the spinal cord in 70% of the cases.44 Other less frequent locations of these cysts include the cerebellopontine angle,29,110 brainstem,9,71,126 and optic nerve.107 Multiple intracranial cysts have also been found.121 Fusion or malformation of the VBs at the level of the cyst can occur in up to 50% of patients, and an association with intramedullary epidermoid cyst, meningomyelocele, spinal lipoma, syringomyelia, diastematomyelia, and a variety of gastrointestinal tract anomalies has been noted, in particular partial duplications of the alimentary tract and fistulas, anal atresia, cardiac anomalies, and renal malformations.6,7,82 In the present series, the cervicothoracic forms were the most common and, in keeping with the literature, the ventral aspect in the spinal canal was the most frequent location.13,21,26,28,35,43,44,46,51,53,55,56,67,72,76,85,86,92,94,99–101,103,108,118–120,124 Computerized tomography scanning and MR imaging may aid in the diagnosis of the neurenteric cyst and associated abnormalities in two aspects, the visualization of the cyst itself and the visualization of any associated abnormality.4,12,52,87 The appearance of the cyst on MR images is that of high protein content without hemorrhage (lower inJ. Neurosurg: Pediatrics / Volume 103 / December, 2005

tensity than the spinal cord, higher intensity than CSF on short repetition time spin echo images).17,36,109 The MR imaging findings in our series revealed that the cyst’s most common aspects were hypointensity on T1-weighted images and hyperintensity on T2-weighted images, which appeared in nine (56.2%) of 16 cases. There is a male predominance (61.2%) in the pediatric cases reported in the literature, and the mean age was 6.4 years, with a median age of 6 years. Clinically, the more complicated lesions tend to present earlier in life. The mediastinal forms can promote respiratory distress in a newborn (treatment consists of excising the mass through a thoracic approach)32,90 or combined neurological symptoms.3,18,105 On neurological presentation patients with these cysts display no characteristic clinical findings, nor is a particular history associated with this disease. Neurologically, the patients present during the first decade of life with pain and myelopathy21,34,75,78,89 arising from spinal cord compression.88 In some cases, neurological signs can be insidious or even absent, despite severe compression of the spinal cord.99,118 Meningitis has been the presenting feature in newborns and infants74 and its symptoms have ranged from low-grade meningeal irritations65 caused by cystic fluid leakage to acute pyogenic meningitis3,49,68 with extensive intraspinal and intramedullary abscesses.74 Meningitis was present in 5.1% of the cases in our review. In one patient (Case 3) we observed an initial diagnosis of retropharyngeal abscess that was surgically addressed five times via the transpharyngeal route. Subsequent referral led to identification of a high-density cystic mass in the clivus region. The neurenteric cyst was removed by the transoral route. The patient made an uneventful recovery and there were no further episodes of meningitis. Similar cases have been described in the literature,68,74 and Ein, et al.,25 described a pediatric case of osteomyelitis of the cervical spine that was mistakenly noted to be a neurenteric cyst initially. In both the pediatric literature and in our series, acute neurological deterioration from neurenteric cysts is common.2,12,24,47,63,64,103,119 We observed an acute presentation in 43.2% of the pediatric cases reviewed. This is thought to be due to sudden mechanical compression of a chronically distorted and compressed spinal cord, or an increase in the size of the cyst as the result of an accumulation of intracystic fluid.75,88,103 In our series, we observed a history of trauma or infection in four patients. The patient in our Case 4 experienced six episodes of meningitis but had normal findings on MR images before suffering a seventh acute meningitis episode, at which time the appearance of the cyst on an MR image enabled a correct diagnosis. The cranial forms of neurenteric cysts are rarer in the pediatric population.45,117 Recently, several authors described only two of 10 pediatric cases occurring in the posterior fossa.33,45 Other authors have described craniocervical cysts.26,48,74 In his personal series on neurenteric cysts, Matson71 described a child with a cyst in the brainstem who died of respiratory failure. We describe four additional intracranial cases (Cases 1–4). Among them, Case 1 seems to be the first instance of a neurenteric cyst of the cavernous sinus described in the pediatric population. Although the literature purports that the goal of treatment of neurenteric cysts is excision,56,60,74,84,89,115 some authors have indicated that tight adherence to the neural structures 519


FIG. 2. Case 6. Two MR images of an anterior cervical spinal cord cyst removed by posterior laminoplasty. Left: Preoperative axial T2-weighted image of the neurenteric cyst. Right: Postoperative midsagittal T2-weighted image demonstrating the total resection of the cyst.

does not permit its safe total removal.21,99,103,122,123 Several authors2,75,77 have described a partial excision of intramedullary cysts. Ergun, et al.,26 described a partial removal of the anterior lesion in the spinal cord with a T-shaped silastic tube catheter placed to drain the residual cavity to the subarachnoid space. These authors recommended a cystosubarachnoid shunt after partial resection to prevent the possibility of severe neurological deficits (including paraplegia or tetraplegia) due to the tight adherence to the neural structures. The surgical approach to the spinal canal is discussed in the literature, with some authors advocating an anterior approach.21 These authors reported that total excision of an anterior cyst via a posterior laminectomy is technically difficult without manipulation of the cord, and they recommended an anterior approach to the ventral lesions of the spinal canal to avoid the recurrence of the cyst. Menezes and Ryken74 reported that the posterior approach, due to limited visualization of the cyst walls and the presence of vascular and VBs, limits the likelihood of complete excision. The optimal surgical strategy remains controversial. The anterior approach is indicated for several reasons: complete resection is easier because the cyst is generally anterior to the spinal cord, and there is less risk of trauma to the spinal cord and of kyphosis. In addition, better management of cases associated with complex vertebral anomalies is possible.5,79,103 In our series, a posterior approach via laminoplasty was chosen as a first surgery in all of the spinal cases (Fig. 2). In all of our patients, it was possible to remove the cyst totally or subtotally without recurrences or clinical deterioration. Except in cases involving previous meningitis (in which adhesions present a problem), the posterior approach can be used as a first surgery. There is a consensus in the literature that the simple aspiration method is unacceptable because it generally results in recurrence of the cyst and is unlikely to yield a pathological diagnosis. Incomplete excision may result in excessive scarring and hamper attempts at a repeated excision when the cyst and symptoms recur.64,74,94 On the other hand, Wilkins and Rossitch123 have indicated that postoperative arachnoiditis is not generally a problem after partial resec520

tion and because neurological improvement usually occurs. If part of the cyst lining remains, the cyst may form again; however, these authors point out that this process may take years to become symptomatic. Some cases of recurrence have been reported in the literature.30,44,45,50,58,59,67,77,80,98 Although total removal of the lesion is not always possible, no documented recurrence after such a procedure has been reported in the literature.94 Chavda, et al.,16 reported a recurrence rate of 37% in a series of eight patients (two of whom were pediatric patients) and all recurrences were found after a partial resection of the cyst. In our pediatric review, a recurrence of the cyst was observed in 14 (11.9%) of 121 patients (there were 16 recurrences in 14 patients). All cases reported on involved partial resection of the cyst. Early detection and treatment will usually lead to complete neurological recovery,66,114 but the outcome is not always optimal and authors have reported deaths.13,18,50,79,82 In our review, complete neurological recovery was observed in 55.5% of the cases, mild or moderate dysfunction in 30.7%, and death or neurological aggravation in 5.9%. Recently, Perry and colleagues91 published reports on widespread craniospinal dissemination associated with the incomplete resection of neurenteric cysts in the posterior fossa, and, in an adult patient, a malignant transformation of a neurenteric cyst that was initially removed in toto in a well-differentiated papillary adenocarcinoma.42,104 Among the 15 survivors in our series, we observed an asymptomatic evolution in 12 patients during the long-term follow-up period. Conclusions Neurenteric cysts are midline lesions that can be localized in any part of the CNS. Magnetic resonance imaging can confirm these cystic lesions and is the imaging method of choice for investigating them. The signs and symptoms of acute spinal cord compression are common. Bone anomalies are also common, and plain x-ray studies or computerized tomography scans should be used to identify these malformations. Complete excision is the aim of surgical inJ. Neurosurg: Pediatrics / Volume 103 / December, 2005

Neurenteric cysts in children tervention. If total removal is achieved, the prognosis is excellent. The spinal cysts in this pediatric series were all approached via the posterior route.

22.

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