J Neurosurg 73:375-382,1990
Craniocervical decompression for cervicomedullary compression in pediatric patients with achondroplasia JOHN ARYANPUR, M.D., OREST HURKO, M.D., CLAIR FRANCOMANO, M.D., HENRY WANG, M.D., AND BENJAMIN CARSON, M.D. Departments of Neurosurgery, Neurology, Medical Genetics, and Neuroradiology, The Johns Hopkins Medical Institutions, Baltimore, Maryland ~," The congenital osseous abnormalities associated with achondroplasia include stenosis of the foramen magnum and the upper cervical spinal canal, In the pediatric achondroplastic patient, such stenosis may lead to cervicomedullary compression with serious sequelae, including paresis, hypertonia, delayed motor milestones, and respiratory compromise. Using a standardized protocol the authors have treated 15 young achondroplastic patients with documented cervicomedullary compression by craniocervical decompression and duroplasty. Following this procedure, significant improvement in presenting neurological or respiratory complaints was noted in all patients. The mortality rate in this series was zero. The major cause of morbidity associated with this procedure was perioperative cerebrospinal fluid (CSF) leakage from the surgical wound, presumably related to coexisting abnormalities of CSF dynamics. This problem was successfully managed by temporary or, when necessary, permanent CSF diversion procedures. It is concluded that craniocervical decompression is an effective and safe treatment for young achondroplastic patients with cervicomedullary compression. KEY WORDS hydrocephalus
9 achondroplasia children
A
9 spinal compression
CHONDROPLASIAis an autosomal-dominant condition characterized by dwarfism, macrocephaly, rhizomelic shortening of the extremities, and other skeletal abnormalities, all resulting from a defect in endochondral bone formation. 16 Neurological dysfunction is frequent in achondroplasia, resulting from compression of the neuraxis at several distinct levels. 4'5"~2'~8"~9In adult achondroplastic patients, spinal stenosis (due primarily to spondylosis in the setting of a congenitally narrowed spinal canal) has become well recognized and its treatment has been described by others. 4"5'j2'~9"2~In the pediatric achondroplastic population, cervicomedullary compression secondary to osseous and ligamentous abnormalities of the foramen magnum and upper cervical spine has been increasingly recognized as a cause of morbidity and mortality.J.6,s,13,17.t8,25 The clinical manifestations of cervicomedullary compression in these patients may be subtle and are often overlooked or mistakenly attributed to coexistent congenital abnormalities. Furthermore, these coexistent malformations often complicate the surgical and anesthetic management of these patients. For this reason,
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9 craniocervical decompression
9
the diagnosis and treatment of clinically significant cervicomedullary compression in this population are not straightforward. Over the period from 1984 to 1989, 15 pediatric patients with achondroplasia and cervicomedullary compression were treated surgically at our institution. Our experience with the management of this difficult group of patients is presented. Clinical Material and Methods
The records of all pediatric patients with heterozygous achondroplasia who were admitted to the Johns Hopkins Hospital for clinical evaluation between 1984 and 1989 were reviewed. Of this group of 58 patients, 15 had undergone craniocervical decompression for cervicomedullary compression. Comprehensive chart reviews were performed for these 15 patients. Clinical Evaluation The clinical evaluation protocol used was standardized for all patients and has been described previously. ~8 In brief, patients were evaluated by a multidisciplinary team including neurosurgeons, pediatric neurologists, 375
J. Aryanpur, et al. pulmonary and sleep specialists, geneticists, anesthesiologists, neuroradiologists, and otolaryngologists. Evaluation in all patients included a detailed neurological and general physical examination as well as assessment of the adequacy of the foramen magnum and upper cervical spine by intrathecally enhanced computerized tomography (CT) or magnetic resonance (MR) imaging techniques. Previous authors9'23 have defined criteria for the radiographic diagnosis of craniocervical stenosis in young patients with achondroplasia. Patients who underwent decompressive surgery fit those criteria. In some patients, axial CT scans or MR images of the head were available and were evaluated for the presence of ventriculomegaly based upon measurement of the bifrontal ventricular size index.l~ Other studies, including cinelaryngology, pulmonary function tests, polysomnography, electromyography, nerve conduction tests, somatosensory evoked potential monitoring, and electroencephalography, were performed as indicated to clarify the diagnosis in selected patients.
Diagnostic Criteria Uniform criteria were applied for the diagnosis of cervicomedullary compression. It should be emphasized that the diagnosis of craniocervical stenosis is purely radiographic and may not imply clinically relevant cervicomedullary compression; however, the diagnosis of cervicomedullary compression relies on both radiographic and clinical factors. The criteria used to establish the diagnosis of cervicomedullary compression included: 1) the presence of signs or symptoms suggestive of ongoing brain-stem compression (such as apnea, lower cranial nerve palsies, hyperreflexia or hypertonia, paresis, or sustained clonus); and 2) radiographic evidence of foramen magnum or upper cervical canal stenosis with or without compression of the neuraxis. In addition, whenever possible the tests described above were used to exclude other possible etiologies of respiratory or neurological dysfunction (such as obstructive respiratory difficulty secondary to oropharyngeal hypoplasia). Because hypotonia and delayed motor milestones are present in nearly all young achondro= plastic patients, is these features were not useful in distinguishing those achondroplastic patients with clinically significant cervicomedullary compression. Surgical Procedure All 15 patients diagnosed as having clinically significant cervicomedullary compression underwent foramen magnum decompression, duroplasty, and upper cervical laminectomy. The surgical procedure has been described previously. 2 Because of several instances of cerebrospinal fluid (CSF) leakage from the surgical wound (see Discussion), the original procedure was modified after the first six patients to include a ventriculostomy prior to the foramen magnum decompression. The ventriculostomy served to divert CSF flow and protect the duroplasty until adequate wound healing could occur. Preoperatively, an external ventricular 376
drain (EVD) was inserted via a right frontal approach into the anterior horn of the right lateral ventricle. The EVD was left in place (closed) throughout the subsequent surgical procedure, and was opened immediately postoperatively to continuous drainage at an intracranial pressure (ICP) of greater than 10 cm H20. The EVD was removed on the 2nd or 3rd postoperative day in all cases. For the craniocervical decompression itself, patients were positioned prone on the operating table with the head and neck carefully supported in slight flexion using a padded pediatric horseshoe headrest. Upper-extremity somatosensory evoked potentials were assessed routinely during positioning as well as during the decompression procedure itself. A midline suboccipital incision was made and subperiosteal dissection performed to expose the occiput and the spinous processes of C-1 and C-2. The arch of C-1 was then removed using a high-speed drill and small curettes. In several patients, compression of the cervical cord necessitated the removal of the arch of C-2 as well. Subsequently, the posterior rim of the foramen magnum was removed with a high-speed drill and small, straight and angled curettes. Invariably, the bone rim of the posterior foramen magnum was greatly thickened and oriented more horizontally than usual, severely indenting the underlying theca. Once the bone decompression was complete, an abnormally thick fibrous band or pannus was often observed at the level of the foramen magnum. Duroplasty was performed by incising the pannus and opening the dura in the midline along the area of constriction. Adequate cord pulsations and CSF flow were confirmed, and a dural patch graft was performed utilizing paraspinous fascia or commercially available human cadaveric dura. The wound was then closed in several layers and, once movement was confirmed in all four extremities, the patients were sent to the pediatric intensive care unit. Extubation was often performed immediately postoperatively; however, in some cases, facial and laryngeal edema delayed extubation for 12 to 24 hours.
Postoperative Evaluation Postoperatively, patients were observed carefully and evaluated for improvement or resolution of presenting signs and symptoms. Serial neurological examinations were performed prior to discharge, and follow-up studies were scheduled as needed. Patients were discharged when stable medically and when all wounds appeared healed. Periodic follow-up data were obtained for all patients, either by return clinic visits or by communication with the referring physician. Resolution or persistence of presenting signs and symptoms was determined, and neurological status assessed. Results
Mean age of these patients at the time of evaluation at our institution was 3.5 years (range 8 months to 18
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Craniocervical decompression in achondroplasia TABLE 1
Summary of clinical characteristics* Preop Duration Ventricof Sx ulomegaly (yrs)
Case No.
Age (yrs), Sex
Surgery
Complications
1
5, F
sleep apnea, rt hemiparesis
3
--
CCD
none
2
1.2, M
apnea & cyanotic episodes
0.66
yes
CCD
none
3
3, M
1
4 5
2, F 2, F
6
2.5, M
apnea, hyperreflexia, quadriparesis, shunted hydrocephalus quadriparesis, hyperreflexia apnea, respiratory arrest • 2, lower-extremity paresis quadriparesis, hyperreflexia
no (previous shunt) no yes
CCD
none
CCD CCD
1
--
CCD
apnea unrelieved by tracheotomy, delayed motor milestones quadriparesis, gait disturbance
0.5
no
CCD with EVD
none CSF leak ~ shunt CSFleak meningitis meningitis
7
2, M
8
4, F
1
yes
CCD with EVD
subdural hygroma --+ shunt
T gait & LE strength
9
1, M
0.25
yes
CCD with EVD
none
apnea gone, ~' tone
4 6
yes yes
CCD with EVD CCD with EVD
none none
1
yes
CCD with EVD
0.25
--
CCD with EVD
CSF leak --* shunt none
14 0.66, M
apnea, respiratory arrest, hypertonia paraparesis, spasticity spasticity, hyperreflexia, severe gait disturbance spasticity, delayed motor milestones, hyperreflexia hypertonia, delayed motor milestones apnea, cyanotic episodes
10 11
9, M 18, F
0.33
yes
CCD with EVD
T gait & LE strength T strength in UE & LE, T gait attaining milestones, hypotonia attaining milestones, walking apnea gone
12
1.25, M
13
1.25, M
15
apnea, paraparesis, hyperreflexia
6
yes
CCD with EVD
9, F
Presenting Sx
0.66 0.5
CSFleak --~ shunt none
Results hemiparesis improved, apnea gone post-tracheotomy apnea gone then returned ---}2nd surgery 1' strength, apnea gone post-T + A T LE strength apnea gone, normal LE strength no change apnea gone, 1"LE strength
apnea gone, ~"strength & reflexes
* Sx = symptoms; CCD = craniocervical decompression; EVD = external ventricular drain; CSF = cerebrospinal fluid; T + A = tonsillectomy and adenoidectomy; LE = lower extremity; UE = upper extremity. - - = not measured; ~ = leading to; I" = improved.
years). H o w e v e r , the m a j o r i t y o f p a t i e n t s h a d b e e n s y m p t o m a t i c for a significant p e r i o d b e f o r e initial evaluation. T h e m e a n d u r a t i o n o f s y m p t o m s p r i o r to evalu a t i o n was 1.6 years (range 3 m o n t h s to 6 years). O f the 15 patients, six w e r e f e m a l e a n d n i n e male.
tients were f o u n d to h a v e p r i m a r i l y o b s t r u c t i v e apnea, three h a d e l e m e n t s o f b o t h central a n d o b s t r u c t i v e apnea, a n d in t w o p a t i e n t s n o a b n o r m a l i t i e s w e r e detected.
Clinical Characteristics
R a d i o g r a p h i c i n v e s t i g a t i o n s typically r e v e a l e d a small, m i s s h a p e n f o r a m e n m a g n u m . F r e q u e n t l y , m e a s u r e m e n t s o f the c o r o n a l a n d mid-sagittal f o r a m e n m a g n u m d i a m e t e r on axial C T scans or M R i m a g e s d e m onstrated dimensions more than 3 standard deviations s m a l l e r t h a n t h o s e o f a g e - m a t c h e d n o r m a l controls. 9 E f f a c e m e n t o f s u b a r a c h n o i d spaces s u r r o u n d i n g the b r a i n s t e m a n d u p p e r cervical spinal c o r d a n d a b n o r m a l p r o t u b e r a n c e o f the o d o n t o i d a n d p o s t e r i o r r i m o f the f o r a m e n m a g n u m w e r e also observed. In several instances, i n d e n t a t i o n or c o m p r e s s i o n o f t h e n e u r a x i s was visualized (Fig. 1 upper pair). M e a s u r e m e n t s o f the b i f r o n t a l v e n t r i c u l a r size i n d e x o n C T scans a n d M R i m a g e s r e v e a l e d v e n t r i c u l o m e g a l y in n i n e o f 12 p a t i e n t s for w h o m these studies were
T h e clinical characteristics o f this p a t i e n t g r o u p are p r e s e n t e d in T a b l e 1. T h e m o s t f r e q u e n t p r e s e n t i n g clinical features were u p p e r - or l o w e r - e x t r e m i t y paresis (10 patients), a p n e a o r cyanosis (eight patients), h y p e r reflexia o r h y p e r t o n i a (eight patients), a n d general d e l a y in m o t o r m i l e s t o n e s e v e n b e y o n d t h a t n o r m a l l y exp e c t e d w i t h a c h o n d r o p l a s i a (three patients). M a n y patients h a d m o r e t h a n o n e p r e s e n t i n g p r o b l e m : the c o n stellation o f m o n o - a n d paraparesis w i t h h y p e r r e f l e x i a a n d e p i s o d i c c y a n o s i s or a p n e a was p a r t i c u l a r l y c o m m o n . S u c h p a t i e n t s p r e s e n t e d a striking c o n t r a s t to the usual floppy, h y p o t o n i c a c h o n d r o p l a s t i c infant. In all eight p a t i e n t s w i t h a history o f c y a n o s i s or a p n e i c episodes, p o l y s o m n o g r a p h y was p e r f o r m e d . T h r e e pa-
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Radiographic Findings
377
J. Aryanpur, et al.
FIG. 1. Left Pair: Computerized tomography scans in one patient. Preoperative intrathecally enhanced scan through the foramen magnum (upper) revealing effacement of the subarachnoid space posteriorly and compression of the cervicomedullary junction secondary to a small, misshapen foramen magnum. Postoperative unenhanced scan (lower) showing the extent of bone decompression. Right Pair: Magnetic resonance images in another patient. Preoperative midsagittal image through the cervicomedullary junction (spin-echo sequence, TR 600 msec, TE 20 msec, upper) demonstrating indentation of the cervicomedullary junction by a prominent posterior lip of the foramen magnum. Postoperative midsagittal image (spin-echo sequence, TR 600 msec, TE 20 msec, lower) showing no further indentation of the neuraxis. An area of low signal intensity within the upper cervical cord, possibly representing a syrinx, is incidentally noted. available. However, none of these patients had preoperative clinical evidence of elevated ICP. Four patients did develop evidence of increased ICP postoperatively (see below) and eventually required permanent CSF diversion. One patient had undergone shunting for symptomatic hydrocephalus several years before developing signs of cervicomedullary compression. A number of patients had radiographic evidence of ventriculomegaly but did not develop symptomatic hydrocephalus postoperatively; thus, in this series there was no obvious correlation between ventriculomegaly and the eventual need for a shunt.
Surgical Results and Complications The mortality rate in this series was zero. The major morbidity of this procedure included a high incidence of CSF leakage from surgical wounds (four patients). In one patient, this leakage was controlled by local measures (oversewing the wound and compressive/occlusive dressings). In the remaining three patients, ven378
triculoperitoneal (VP) shunting was eventually required to control the hydrocephalus that was responsible for continued leakage. After the first six patients in the series had been treated and the problem of CSF leakage from surgical wounds was identified (two of these patients developed leakage from the suboccipital wound and one required a shunt), the procedure was modified to include controlled perioperative CSF diversion via an EVD. The subsequently treated nine patients underwent both foramen magnum decompression and ventricular drainage via an EVD. The EVD protected the suboccipital suture line well: no patient treated with perioperative CSF diversion developed CSF leakage from the suboccipital wound. Interestingly, however, two patients in this later group developed CSF leakage from the site of the EVD itself. Both of these patients eventually required CSF shunting procedures to control this problem. Intracranial pressure was monitored while the EVD was in place. Periodic resting ICP spikes to 30 to
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Craniocervical decompression in achondroplasia 50 mm Hg were noted in several patients without apparent Valsalva maneuvers or stimulation; however, plateau elevations of ICP were uncommon. While the small sample size did not permit correlation of ICP readings with the eventual need for ventricular shunting, relatively high ICP values and more frequent ICP spikes were observed in one patient who eventually went on to require a shunt. Two patients developed postoperative Gram-negative meningitis (one with and one without demonstrated CSF leakage from the wound); this condition was successfully controlled with antibiotics in both cases. A single patient developed symptomatic bilateral subdural hygromas subsequent to VP shunt placement; these resolved after switching to a higher-pressure shunt system and shunting the subdural space. Clinical Follow- Up Review The mean follow-up period was 19.1 months (range 2 months to 5 years). One patient was lost to follow-up review after the first postoperative visit and is excluded from analysis. At the last follow-up contact, no patient had suffered clinical deterioration following surgery. Improvement or resolution of presenting signs or symptoms was noted in all 14 patients with follow-up data. A breakdown of surgical results by presenting symptom reveals that nine of 10 patients who presented with paresis showed significant improvement in strength postoperatively, some returning to normal. Three children who presented with delayed motor milestones but no other neurological deficits began to attain milestones rapidly following surgery. Six of the eight patients with hyperreflexia or hypertonia demonstrated resolution of these signs postoperatively. Finally, of the eight patients who presented with cyanosis or apnea, six had total resolution of these respiratory problems by the time of last follow-up, whereas two continued to have episodes of cyanosis or apnea even after foramen magnum decompression; these two children were discovered to have an additional component of obstructive apnea which in both cases resolved following surgery directed toward the cause of the obstruction. One patient did well initially, only to develop recurrence of apnea some 3 years following surgery. Subsequent evaluation revealed incomplete decompression of the foramen magnum; repeat craniocervical decompression resulted in total resolution of symptoms. Radiographic Follow- Up Findings
In several patients, follow-up radiological studies were performed to evaluate the adequacy of decompression. These studies typically showed a wide decompression with no residual craniocervical stenosis or brain-stem compression (Fig. 1 lower pair). Discussion
The neurological sequelae of compression of the neuraxis in achondroplastic dwarfs have been well deJ. Neurosurg. / Volume 73/September, 1990
scribed. As early as 1952, Spillane 2~reported three cases of achondroplastic dwarfism with lower-extremity paralysis secondary to spinal cord stenosis. Many subsequent reports have served to define both the condition and its surgical treatment by decompressive laminec-
tomy.4,5,12,19
Cervicomedullary Compression A more dangerous and, until recently, relatively unrecognized form of compression of the neuraxis in achondroplastic patients is compression of the brain stem and upper cervical cord at the level of the foramen magnum. This condition has gained increasing attention as a cause of respiratory and neurological impairment in the pediatric achondroplastic population. ~.6,~3.,7,18,24,25Reid, el al., ~8in a prospective evaluation of achondroplastic infants, found radiographic evidence of craniocervical stenosis in 60% of the pediatric achondroplastic patients they studied. More significantly, 35% of their patients had clinical evidence of cervicomedullary compression. The natural history of this condition has not been systematically studied; however, anecdotal clinical and pathological evidence suggests that the condition may be progressive and frequently lethal. 1'7"8'~3'~8'25Several studies have shown an increased incidence of sudden death in achondroplastic dwarfs under 4 years of age. ~'8"~7In these studies, the increased mortality in this age group has been attributed directly to acute compression of the brain stem and upper cervical cord. Hecht, et al., 8 calculated a 7.5% risk of sudden death in achondroplastic patients during the 1st year of life, a risk calculated to be at least three times greater than that of the general population. 17 Craniocervical Decompression Given this relatively bleak picture, several centers have performed craniocervical decompression on achondroplastic infants with cervicomedullary compression, generally obtaining good results. 6'~3'~8'24 Frequent screening of young patients with achondroplasia for respiratory and neurological impairment and performing early decompression in cases of proven cervicomedullary compression have therefore been recommended. 6'~8'24 Unfortunately, the small numbers of surgical patients in these studies and the lack of follow-up data over a longer period have not allowed a more definitive assessment of the efficacy of this treatment in individuals with heterozygous achondroplasia. Evidence supporting surgical intervention in patients with homozygous achondroplasia is even scantier. ~4 The present study, although necessarily limited by its retrospective nature, provides data by which to evaluate the efficacy of craniocervical decompression in young achondroplastic patients with cervicomedullary compression. As our results indicate, decompression of the cervicomedullary junction in these patients will often bring about a dramatic and sustained improvement in neurological and respiratory function. No patient in our
379
J. Aryanpur, et al. series suffered a decline in neurological status following the procedure. All patients who presented with primarily motor findings were improved postoperatively. Rapid attainment of motor milestones and resolution of hyperreflexia and hypertonia were common. Apnea or cyanosis was a common presenting problem and was corrected in six of the eight patients so afflicted by craniocervical decompression. The remaining two patients improved following surgery directed toward coexistent obstructive respiratory problems. Thus, craniocervical decompression is an effective treatment for cervicomedullary compression in young patients with achondroplasia.
Respiratory Compromise A previous studyTM has reported a 35% incidence of respiratory difficulties in pediatric achondroplastic patients. In some of these patients, respiratory abnormalities were not suspected by referring physicians or parents, and were only detected after workup for unrelated problems. Our results confirm that respiratory dysfunction is a common problem in pediatric achondroplastic patients, and one which may indicate ongoing brainstem compression. In achondroplastic patients, respiratory compromise may be caused by any of several different mechanisms. Purely obstructive etiologies, including upper airway obstruction secondary to micrognathia, facial and laryngeal hypoplasia, and hypotonia of laryngeal musculature, are common. 11,18.22Restrictive pulmonary disease caused by thoracic cage and chest wall deformities may also contribute to respiratory compromise. 18'2z Compression of brain-stem respiratory centers by a small foramen magnum can interfere with central respiratory drive, causing central apnea. 6'~7'18.22In addition, compression of the brain stem and upper cervical cord may directly compress the lower motor neuron systems controlling respiratory muscles, resulting in weak, ineffective respirations. 8"22 Because primary and neurogenic causes of respiratory dysfunction may coexist in the same patient, differentiation between these forms of respiratory compromise is important but often difficult. Patients with primarily obstructive or restrictive pulmonary disease would not be expected to benefit from craniocervical decompression. Conversely, apnea of central origin would not be improved by efforts directed toward a coexistent but minor obstructive component. One of our patients had undergone tracheostomy prior to craniocervical decompression without relief of respiratory difficulties. Two of our patients with cervicomedullary compression required tracheostomy or tonsillectomy and adenoidectomy subsequent to craniocervical decompression because of concomitant obstructive respiratory compromise. Thus, treatment of both obstructive and central apnea may be necessary in this group of patients. Our experience suggests that the coordinated efforts of experienced pediatricians, neurologists, neurosurgeons, radiologists, otolaryngologists, and pulmonologists are vital in deter380
mining which achondroplastic children may benefit from foramen magnum decompression.
Motor Deficits Although the most dangerous consequence of cervicomedullary compression is respiratory arrest via mechanisms described above, other neurological deficits may result from compression of descending and ascending white matter tracts. Hypertonia, upper- and lower-extremity weakness, and spasticity have all been described. 7'13'24'25 Long-standing compression may result in irreversible spinal cord changes and a fixed deficit. 7'25 For this reason, early decompression is recommended in all proven cases of cervicomedullary compression. Pathogenesis of Foramen Magnum Stenosis The pathogenesis of foramen magnum stenosis in achondroplastic patients appears to be related to the generalized defect in endochondral bone formation. ~3 This results in an abnormally small posterior fossa with an extremely horizontally oriented posterior rim. Typically, the posterior lip of the foramen magnum itself is thickened and indents the cervicomedullaryjunction. In addition, a thick band of connective tissue often constricts the theca further at the foramen magnum. Wang, et al.,23 and Hecht, et al.,9 have studied the CT appearance of craniocervical junction abnormalities in pediatric achondroplastic patients. A small, teardropshaped foramen magnum was characteristic. In the study by Wang, et al., 96% of patients evaluated had sagittal and coronal foramen magnum dimensions at least 3 standard deviation smaller than those of agematched control individuals. Surgical Decompression Relief of cervicomedullary compression requires removal of both the osseous and soft-tissue constrictive elements. The use of the high-speed drill provides for rapid controlled removal of bone around the cervicomedullary junction, and should be considered an essential part of the procedure. Removal of bone alone is in general not sufficient to relieve the compression, however. In many cases the release of thick dural constricting bands was required to allow free CSF flow and pulsation around the brain stem and upper cervical cord. Since it is difficult to evaluate the degree of dural impingement upon the cervicomedullary junction by simple inspection, we recommend that the dura be opened in all cases and that patch duroplasty be performed when dural constriction exists. Cerebrospinal Fluid Dynamics Unfortunately, the dural opening required to achieve adequate decompression was also the cause of the major early morbidity associated with this procedure, namely CSF leakage from the surgical wound. Despite meticulous attention to the dural closure techniques, two patients developed postoperative CSF leakage from the suboccipital incision. Under ordinary circumstances a J. Neurosurg. / Volume 73/September, 1990
Craniocervical decompression in achondroplasia properly closed dural suture line would be expected to be watertight; however, it is well recognized that, in achondroplastic patients, CSF dynamics are often abnormal. ~5'2~'24In these patients, ventriculomegaly, abnormally capacious subarachnoid spaces over the cerebral convexities, elevated ICP, and even frank hydrocephalus may' be observed. 15"2~-24 The etiology of the abnormal CSF dynamics associated with achondroplasia is not clear; however, recent work points to stenosis of skull outlet foramina and consequent increased jugular and intracranial venous pressures as a prime causative factor. 21 In the achondroplastic patient with ventriculomegaly but without clear-cut symptomatic hydrocephalus, ventricular shunting is probably best avoided as evidence exists that the condition is not progressive in most patients. 3"24Unfortunately, a significant percentage of achondroplastic patients will eventually develop symptomatic hydrocephalus and require a shunting procedure, At least nine of the 15 patients in the present study had evidence of ventriculomegaly on CT scans or MR images, and four eventually underwent shunt placement. Ventriculomegaly alone need not signi~ Tactive hydrocephalus: however, it probably does indicate a common underlying abnormality of CSF dynamics which, in some patients, may progress to symptomatic hydrocephalus. The high incidence of postoperative CSF leakage from the suboccipital wound in the early cases in this series probably reflected the tendency toward elevated ICP in these patients. Undoubtedly, the inherent friability of pediatric skin and subcutaneous tissues further compounded the problem by providing a weak barrier against elevated CSF pressures. The institution of controlled perioperative CSF diversion via ventriculostomy in the later patients in this series dramatically reduced the incidence of suboccipital wound CSF leakage. In an analogous situation, shunt placement in the newborn with hydrocephalus and a repaired myelomeningocele protects the myelomeningocele wound. Development of CSF leakage from the EVD site itself in two later patients further underscores the existence of abnormal CSF dynamics in patients with achondroplasia, as we have not encountered this problem in individuals with normal CSF dynamics. In addition to CSF diversion, the ability to monitor ICP postoperatively may yield information important in determining which patients might ultimately need shunt placement. Thus, the benefits of perioperative ventriculostomy appear to outweigh the risks associated with the procedure in this group of patients. Conclusions
The treatment of pediatric achondroptastic patients is challenging and requires a coordinated multidisciplinary approach. Although a condition not frequently encountered, the high incidence of compression of the neuraxis and its dangerous sequelae in this patient population mandate familiarity with the available therJ. Neurosurg. / Volume 73/September, 1990
apies. In documented cases of cervicomedullary compression in pediatric achondroplastic patients, early surgical decompression utilizing the techniques described above appears to improve significantly the natural history of this condition. References
1. Bland JD, Emery JL: Unexpected death of children with achondroplasia after the perinatal period. Dev Med Child Neurol 24:489-492, 1982 2. Carson B, Winfield J, Wang H, et al: Surgical management ofcervico-medullary compression in achondroplastic patients, in Nicoletti B, Kopits SE, Ascani E, et al (eds): Human Aehondroplasia. New York: Plenum Press, 1988, pp 207-214 3. Cohen ME, Rosenthal AD, Matson DD: Neurological abnormalities in achondroplastic children. J Pediatr 71: 367-376, 1967 4. Duvoisin RC, Yahr MD: Compressive spinal cord and root syndromes in achondroplastic dwarfs. Neurology 12: 202-207, 1962 5. Epstein JA, Malis LI: Compression of spinal cord and cauda equina in achondroptastic dwarfs. Neurology 5: 875-881, 1955 6. Fremion AS, Garg BP, Kalsbeck J: Apnea as the sole manifestation of cord compression in achondroplasia. J Pediatr 104:398-401, 1984 7. Hecht JT, Butler IJ, Scott CI Jr: Long-term neurological sequelae in achondroplasia. Eur J Pediatr 143:58-60, 1984
8. Hecht JT, Francomano CA, Horton WA, et al: Mortality in achondroplasia. Am J Hum Genet 41:454-464, 1987 9. Hecht JT, Nelson FW, Butler IJ, et al: Computerized tomography of the foramen magnum: achondroplastic values compared to normal standards. Am J Med Genet 20:355-360, 1985 10. Heinz ER, Ward A, Drayer BP, et al: Distinction between obstructive and atrophic dilatation of ventricles in children. J Comput Assist Tomogr 4:320-325, 1980 I 1. Larsen PD, Synder EW, Matsuo F, et al: Achondroplasia associated with obstructive sleep apnea. Arch Neurol 40:769, 1983 (Letter) 12. Lutter LD, Langer LO: Neurological symptoms in achondroplastic dwarfs - - surgical treatment. J Bone Joint Surg (Am) 59:87-92, 1977 13. Luyendijk W, Matricali B, Thomeer RTWM: Basilar impression in an achondroplastic dwarf: causative role in tetraparesis. Acta Neurochir 41:243-253, 1978 14. Moskowitz N, Carson B, Kopits S, et al: Foramen magnum decompression in an infant with homozygous achondroplasia. Case report. J Neurosurg 70:t26-128, 1989 15. Mueller SM, Bell W, Cornell S, et al: Achondroplasia and hydrocephalus. Neurology 27:430-434, 1977 16. Oberklaid F, Danks DM, Jensen F, et al: Achondroplasia and hydrochondroplasia. Comments on frequency, mutation rate, and radiological features in skull and spine. J Med Genet 16:140-146, 1979 17. Pauli RM, Scott CI, Wassman ER Jr, et al: Apnea and sudden unexpected death in infants with achondroplasia. J Pediatr 104:342-348, 1984 18. Reid CS, Pyeritz RE, Kopits SE, et al: Cervicomedullary compression in young patients with achondroplasia: value of comprehensive neurologic and respiratory evaluation. J Pediatr 110:522-530, 1987 19. Shikata J, Yamamuro T, Iida H, et al: Surgical treatment of achondroplastic dwarfs with paraplegia. Surg Neurol 381
J. Aryanpur, et al. 29:125-130, 1988 20. Spillane JD: Three cases of achondroplasia with neurological complications. J Neurol Neurosurg Psychiatry 15: 246-252, 1952 21. Steinbok P, Halt J, Flodmark O: Hydrocephalus in achondroplasia: the possible role of intracranial venous hypertension. J Neurosurg 71:42-48, 1989 22. Stokes DC, Phillips JA, Leonard CO, et al: Respiratory complications of achondroplasia. J Pediatr 102: 534-541, 1983 23. Wang H, Rosenbaum AE, Reid CS, et al: Pediatric patients with achondroplasia: CT evaluation of the craniocervical junction. Radiology 164:515-519, 1987 24. Yamada H, Nakamura S, Tajima M, et al: Neurological manifestations of pediatric achondroplasia. J Neurosurg 54:49-57, 1981
382
25. Yang SS, Corbett DP, Brough AJ, et al: Upper cervical myelopathy in achondroplasia. Am J Clin Pathol 68: 68-72, 1977
Manuscript received November I, 1989. Accepted in final form February 5, 1990. Address reprint requests to." John Aryanpur, M.D., Department of Neurosurgery, Meyer 7-109, The Johns Hopkins Hospital, 600 North Wolfe Street, Baltimore, Maryland 21205.
J. Neurosurg. / Volume 73/S(Tlember, I990
Craniocervical decompression for cervicomedullary compression in pediatric patients with achondroplasia JOHN ARYANPUR, M.D., OREST HURKO, M.D., CLAIR FRANCOMANO, M.D., HENRY WANG, M.D., AND BENJAMIN CARSON, M.D. Departments of Neurosurgery, Neurology, Medical Genetics, and Neuroradiology, The Johns Hopkins Medical Institutions, Baltimore, Maryland ~," The congenital osseous abnormalities associated with achondroplasia include stenosis of the foramen magnum and the upper cervical spinal canal, In the pediatric achondroplastic patient, such stenosis may lead to cervicomedullary compression with serious sequelae, including paresis, hypertonia, delayed motor milestones, and respiratory compromise. Using a standardized protocol the authors have treated 15 young achondroplastic patients with documented cervicomedullary compression by craniocervical decompression and duroplasty. Following this procedure, significant improvement in presenting neurological or respiratory complaints was noted in all patients. The mortality rate in this series was zero. The major cause of morbidity associated with this procedure was perioperative cerebrospinal fluid (CSF) leakage from the surgical wound, presumably related to coexisting abnormalities of CSF dynamics. This problem was successfully managed by temporary or, when necessary, permanent CSF diversion procedures. It is concluded that craniocervical decompression is an effective and safe treatment for young achondroplastic patients with cervicomedullary compression. KEY WORDS hydrocephalus
9 achondroplasia children
A
9 spinal compression
CHONDROPLASIAis an autosomal-dominant condition characterized by dwarfism, macrocephaly, rhizomelic shortening of the extremities, and other skeletal abnormalities, all resulting from a defect in endochondral bone formation. 16 Neurological dysfunction is frequent in achondroplasia, resulting from compression of the neuraxis at several distinct levels. 4'5"~2'~8"~9In adult achondroplastic patients, spinal stenosis (due primarily to spondylosis in the setting of a congenitally narrowed spinal canal) has become well recognized and its treatment has been described by others. 4"5'j2'~9"2~In the pediatric achondroplastic population, cervicomedullary compression secondary to osseous and ligamentous abnormalities of the foramen magnum and upper cervical spine has been increasingly recognized as a cause of morbidity and mortality.J.6,s,13,17.t8,25 The clinical manifestations of cervicomedullary compression in these patients may be subtle and are often overlooked or mistakenly attributed to coexistent congenital abnormalities. Furthermore, these coexistent malformations often complicate the surgical and anesthetic management of these patients. For this reason,
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9 craniocervical decompression
9
the diagnosis and treatment of clinically significant cervicomedullary compression in this population are not straightforward. Over the period from 1984 to 1989, 15 pediatric patients with achondroplasia and cervicomedullary compression were treated surgically at our institution. Our experience with the management of this difficult group of patients is presented. Clinical Material and Methods
The records of all pediatric patients with heterozygous achondroplasia who were admitted to the Johns Hopkins Hospital for clinical evaluation between 1984 and 1989 were reviewed. Of this group of 58 patients, 15 had undergone craniocervical decompression for cervicomedullary compression. Comprehensive chart reviews were performed for these 15 patients. Clinical Evaluation The clinical evaluation protocol used was standardized for all patients and has been described previously. ~8 In brief, patients were evaluated by a multidisciplinary team including neurosurgeons, pediatric neurologists, 375
J. Aryanpur, et al. pulmonary and sleep specialists, geneticists, anesthesiologists, neuroradiologists, and otolaryngologists. Evaluation in all patients included a detailed neurological and general physical examination as well as assessment of the adequacy of the foramen magnum and upper cervical spine by intrathecally enhanced computerized tomography (CT) or magnetic resonance (MR) imaging techniques. Previous authors9'23 have defined criteria for the radiographic diagnosis of craniocervical stenosis in young patients with achondroplasia. Patients who underwent decompressive surgery fit those criteria. In some patients, axial CT scans or MR images of the head were available and were evaluated for the presence of ventriculomegaly based upon measurement of the bifrontal ventricular size index.l~ Other studies, including cinelaryngology, pulmonary function tests, polysomnography, electromyography, nerve conduction tests, somatosensory evoked potential monitoring, and electroencephalography, were performed as indicated to clarify the diagnosis in selected patients.
Diagnostic Criteria Uniform criteria were applied for the diagnosis of cervicomedullary compression. It should be emphasized that the diagnosis of craniocervical stenosis is purely radiographic and may not imply clinically relevant cervicomedullary compression; however, the diagnosis of cervicomedullary compression relies on both radiographic and clinical factors. The criteria used to establish the diagnosis of cervicomedullary compression included: 1) the presence of signs or symptoms suggestive of ongoing brain-stem compression (such as apnea, lower cranial nerve palsies, hyperreflexia or hypertonia, paresis, or sustained clonus); and 2) radiographic evidence of foramen magnum or upper cervical canal stenosis with or without compression of the neuraxis. In addition, whenever possible the tests described above were used to exclude other possible etiologies of respiratory or neurological dysfunction (such as obstructive respiratory difficulty secondary to oropharyngeal hypoplasia). Because hypotonia and delayed motor milestones are present in nearly all young achondro= plastic patients, is these features were not useful in distinguishing those achondroplastic patients with clinically significant cervicomedullary compression. Surgical Procedure All 15 patients diagnosed as having clinically significant cervicomedullary compression underwent foramen magnum decompression, duroplasty, and upper cervical laminectomy. The surgical procedure has been described previously. 2 Because of several instances of cerebrospinal fluid (CSF) leakage from the surgical wound (see Discussion), the original procedure was modified after the first six patients to include a ventriculostomy prior to the foramen magnum decompression. The ventriculostomy served to divert CSF flow and protect the duroplasty until adequate wound healing could occur. Preoperatively, an external ventricular 376
drain (EVD) was inserted via a right frontal approach into the anterior horn of the right lateral ventricle. The EVD was left in place (closed) throughout the subsequent surgical procedure, and was opened immediately postoperatively to continuous drainage at an intracranial pressure (ICP) of greater than 10 cm H20. The EVD was removed on the 2nd or 3rd postoperative day in all cases. For the craniocervical decompression itself, patients were positioned prone on the operating table with the head and neck carefully supported in slight flexion using a padded pediatric horseshoe headrest. Upper-extremity somatosensory evoked potentials were assessed routinely during positioning as well as during the decompression procedure itself. A midline suboccipital incision was made and subperiosteal dissection performed to expose the occiput and the spinous processes of C-1 and C-2. The arch of C-1 was then removed using a high-speed drill and small curettes. In several patients, compression of the cervical cord necessitated the removal of the arch of C-2 as well. Subsequently, the posterior rim of the foramen magnum was removed with a high-speed drill and small, straight and angled curettes. Invariably, the bone rim of the posterior foramen magnum was greatly thickened and oriented more horizontally than usual, severely indenting the underlying theca. Once the bone decompression was complete, an abnormally thick fibrous band or pannus was often observed at the level of the foramen magnum. Duroplasty was performed by incising the pannus and opening the dura in the midline along the area of constriction. Adequate cord pulsations and CSF flow were confirmed, and a dural patch graft was performed utilizing paraspinous fascia or commercially available human cadaveric dura. The wound was then closed in several layers and, once movement was confirmed in all four extremities, the patients were sent to the pediatric intensive care unit. Extubation was often performed immediately postoperatively; however, in some cases, facial and laryngeal edema delayed extubation for 12 to 24 hours.
Postoperative Evaluation Postoperatively, patients were observed carefully and evaluated for improvement or resolution of presenting signs and symptoms. Serial neurological examinations were performed prior to discharge, and follow-up studies were scheduled as needed. Patients were discharged when stable medically and when all wounds appeared healed. Periodic follow-up data were obtained for all patients, either by return clinic visits or by communication with the referring physician. Resolution or persistence of presenting signs and symptoms was determined, and neurological status assessed. Results
Mean age of these patients at the time of evaluation at our institution was 3.5 years (range 8 months to 18
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Craniocervical decompression in achondroplasia TABLE 1
Summary of clinical characteristics* Preop Duration Ventricof Sx ulomegaly (yrs)
Case No.
Age (yrs), Sex
Surgery
Complications
1
5, F
sleep apnea, rt hemiparesis
3
--
CCD
none
2
1.2, M
apnea & cyanotic episodes
0.66
yes
CCD
none
3
3, M
1
4 5
2, F 2, F
6
2.5, M
apnea, hyperreflexia, quadriparesis, shunted hydrocephalus quadriparesis, hyperreflexia apnea, respiratory arrest • 2, lower-extremity paresis quadriparesis, hyperreflexia
no (previous shunt) no yes
CCD
none
CCD CCD
1
--
CCD
apnea unrelieved by tracheotomy, delayed motor milestones quadriparesis, gait disturbance
0.5
no
CCD with EVD
none CSF leak ~ shunt CSFleak meningitis meningitis
7
2, M
8
4, F
1
yes
CCD with EVD
subdural hygroma --+ shunt
T gait & LE strength
9
1, M
0.25
yes
CCD with EVD
none
apnea gone, ~' tone
4 6
yes yes
CCD with EVD CCD with EVD
none none
1
yes
CCD with EVD
0.25
--
CCD with EVD
CSF leak --* shunt none
14 0.66, M
apnea, respiratory arrest, hypertonia paraparesis, spasticity spasticity, hyperreflexia, severe gait disturbance spasticity, delayed motor milestones, hyperreflexia hypertonia, delayed motor milestones apnea, cyanotic episodes
10 11
9, M 18, F
0.33
yes
CCD with EVD
T gait & LE strength T strength in UE & LE, T gait attaining milestones, hypotonia attaining milestones, walking apnea gone
12
1.25, M
13
1.25, M
15
apnea, paraparesis, hyperreflexia
6
yes
CCD with EVD
9, F
Presenting Sx
0.66 0.5
CSFleak --~ shunt none
Results hemiparesis improved, apnea gone post-tracheotomy apnea gone then returned ---}2nd surgery 1' strength, apnea gone post-T + A T LE strength apnea gone, normal LE strength no change apnea gone, 1"LE strength
apnea gone, ~"strength & reflexes
* Sx = symptoms; CCD = craniocervical decompression; EVD = external ventricular drain; CSF = cerebrospinal fluid; T + A = tonsillectomy and adenoidectomy; LE = lower extremity; UE = upper extremity. - - = not measured; ~ = leading to; I" = improved.
years). H o w e v e r , the m a j o r i t y o f p a t i e n t s h a d b e e n s y m p t o m a t i c for a significant p e r i o d b e f o r e initial evaluation. T h e m e a n d u r a t i o n o f s y m p t o m s p r i o r to evalu a t i o n was 1.6 years (range 3 m o n t h s to 6 years). O f the 15 patients, six w e r e f e m a l e a n d n i n e male.
tients were f o u n d to h a v e p r i m a r i l y o b s t r u c t i v e apnea, three h a d e l e m e n t s o f b o t h central a n d o b s t r u c t i v e apnea, a n d in t w o p a t i e n t s n o a b n o r m a l i t i e s w e r e detected.
Clinical Characteristics
R a d i o g r a p h i c i n v e s t i g a t i o n s typically r e v e a l e d a small, m i s s h a p e n f o r a m e n m a g n u m . F r e q u e n t l y , m e a s u r e m e n t s o f the c o r o n a l a n d mid-sagittal f o r a m e n m a g n u m d i a m e t e r on axial C T scans or M R i m a g e s d e m onstrated dimensions more than 3 standard deviations s m a l l e r t h a n t h o s e o f a g e - m a t c h e d n o r m a l controls. 9 E f f a c e m e n t o f s u b a r a c h n o i d spaces s u r r o u n d i n g the b r a i n s t e m a n d u p p e r cervical spinal c o r d a n d a b n o r m a l p r o t u b e r a n c e o f the o d o n t o i d a n d p o s t e r i o r r i m o f the f o r a m e n m a g n u m w e r e also observed. In several instances, i n d e n t a t i o n or c o m p r e s s i o n o f t h e n e u r a x i s was visualized (Fig. 1 upper pair). M e a s u r e m e n t s o f the b i f r o n t a l v e n t r i c u l a r size i n d e x o n C T scans a n d M R i m a g e s r e v e a l e d v e n t r i c u l o m e g a l y in n i n e o f 12 p a t i e n t s for w h o m these studies were
T h e clinical characteristics o f this p a t i e n t g r o u p are p r e s e n t e d in T a b l e 1. T h e m o s t f r e q u e n t p r e s e n t i n g clinical features were u p p e r - or l o w e r - e x t r e m i t y paresis (10 patients), a p n e a o r cyanosis (eight patients), h y p e r reflexia o r h y p e r t o n i a (eight patients), a n d general d e l a y in m o t o r m i l e s t o n e s e v e n b e y o n d t h a t n o r m a l l y exp e c t e d w i t h a c h o n d r o p l a s i a (three patients). M a n y patients h a d m o r e t h a n o n e p r e s e n t i n g p r o b l e m : the c o n stellation o f m o n o - a n d paraparesis w i t h h y p e r r e f l e x i a a n d e p i s o d i c c y a n o s i s or a p n e a was p a r t i c u l a r l y c o m m o n . S u c h p a t i e n t s p r e s e n t e d a striking c o n t r a s t to the usual floppy, h y p o t o n i c a c h o n d r o p l a s t i c infant. In all eight p a t i e n t s w i t h a history o f c y a n o s i s or a p n e i c episodes, p o l y s o m n o g r a p h y was p e r f o r m e d . T h r e e pa-
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Radiographic Findings
377
J. Aryanpur, et al.
FIG. 1. Left Pair: Computerized tomography scans in one patient. Preoperative intrathecally enhanced scan through the foramen magnum (upper) revealing effacement of the subarachnoid space posteriorly and compression of the cervicomedullary junction secondary to a small, misshapen foramen magnum. Postoperative unenhanced scan (lower) showing the extent of bone decompression. Right Pair: Magnetic resonance images in another patient. Preoperative midsagittal image through the cervicomedullary junction (spin-echo sequence, TR 600 msec, TE 20 msec, upper) demonstrating indentation of the cervicomedullary junction by a prominent posterior lip of the foramen magnum. Postoperative midsagittal image (spin-echo sequence, TR 600 msec, TE 20 msec, lower) showing no further indentation of the neuraxis. An area of low signal intensity within the upper cervical cord, possibly representing a syrinx, is incidentally noted. available. However, none of these patients had preoperative clinical evidence of elevated ICP. Four patients did develop evidence of increased ICP postoperatively (see below) and eventually required permanent CSF diversion. One patient had undergone shunting for symptomatic hydrocephalus several years before developing signs of cervicomedullary compression. A number of patients had radiographic evidence of ventriculomegaly but did not develop symptomatic hydrocephalus postoperatively; thus, in this series there was no obvious correlation between ventriculomegaly and the eventual need for a shunt.
Surgical Results and Complications The mortality rate in this series was zero. The major morbidity of this procedure included a high incidence of CSF leakage from surgical wounds (four patients). In one patient, this leakage was controlled by local measures (oversewing the wound and compressive/occlusive dressings). In the remaining three patients, ven378
triculoperitoneal (VP) shunting was eventually required to control the hydrocephalus that was responsible for continued leakage. After the first six patients in the series had been treated and the problem of CSF leakage from surgical wounds was identified (two of these patients developed leakage from the suboccipital wound and one required a shunt), the procedure was modified to include controlled perioperative CSF diversion via an EVD. The subsequently treated nine patients underwent both foramen magnum decompression and ventricular drainage via an EVD. The EVD protected the suboccipital suture line well: no patient treated with perioperative CSF diversion developed CSF leakage from the suboccipital wound. Interestingly, however, two patients in this later group developed CSF leakage from the site of the EVD itself. Both of these patients eventually required CSF shunting procedures to control this problem. Intracranial pressure was monitored while the EVD was in place. Periodic resting ICP spikes to 30 to
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Craniocervical decompression in achondroplasia 50 mm Hg were noted in several patients without apparent Valsalva maneuvers or stimulation; however, plateau elevations of ICP were uncommon. While the small sample size did not permit correlation of ICP readings with the eventual need for ventricular shunting, relatively high ICP values and more frequent ICP spikes were observed in one patient who eventually went on to require a shunt. Two patients developed postoperative Gram-negative meningitis (one with and one without demonstrated CSF leakage from the wound); this condition was successfully controlled with antibiotics in both cases. A single patient developed symptomatic bilateral subdural hygromas subsequent to VP shunt placement; these resolved after switching to a higher-pressure shunt system and shunting the subdural space. Clinical Follow- Up Review The mean follow-up period was 19.1 months (range 2 months to 5 years). One patient was lost to follow-up review after the first postoperative visit and is excluded from analysis. At the last follow-up contact, no patient had suffered clinical deterioration following surgery. Improvement or resolution of presenting signs or symptoms was noted in all 14 patients with follow-up data. A breakdown of surgical results by presenting symptom reveals that nine of 10 patients who presented with paresis showed significant improvement in strength postoperatively, some returning to normal. Three children who presented with delayed motor milestones but no other neurological deficits began to attain milestones rapidly following surgery. Six of the eight patients with hyperreflexia or hypertonia demonstrated resolution of these signs postoperatively. Finally, of the eight patients who presented with cyanosis or apnea, six had total resolution of these respiratory problems by the time of last follow-up, whereas two continued to have episodes of cyanosis or apnea even after foramen magnum decompression; these two children were discovered to have an additional component of obstructive apnea which in both cases resolved following surgery directed toward the cause of the obstruction. One patient did well initially, only to develop recurrence of apnea some 3 years following surgery. Subsequent evaluation revealed incomplete decompression of the foramen magnum; repeat craniocervical decompression resulted in total resolution of symptoms. Radiographic Follow- Up Findings
In several patients, follow-up radiological studies were performed to evaluate the adequacy of decompression. These studies typically showed a wide decompression with no residual craniocervical stenosis or brain-stem compression (Fig. 1 lower pair). Discussion
The neurological sequelae of compression of the neuraxis in achondroplastic dwarfs have been well deJ. Neurosurg. / Volume 73/September, 1990
scribed. As early as 1952, Spillane 2~reported three cases of achondroplastic dwarfism with lower-extremity paralysis secondary to spinal cord stenosis. Many subsequent reports have served to define both the condition and its surgical treatment by decompressive laminec-
tomy.4,5,12,19
Cervicomedullary Compression A more dangerous and, until recently, relatively unrecognized form of compression of the neuraxis in achondroplastic patients is compression of the brain stem and upper cervical cord at the level of the foramen magnum. This condition has gained increasing attention as a cause of respiratory and neurological impairment in the pediatric achondroplastic population. ~.6,~3.,7,18,24,25Reid, el al., ~8in a prospective evaluation of achondroplastic infants, found radiographic evidence of craniocervical stenosis in 60% of the pediatric achondroplastic patients they studied. More significantly, 35% of their patients had clinical evidence of cervicomedullary compression. The natural history of this condition has not been systematically studied; however, anecdotal clinical and pathological evidence suggests that the condition may be progressive and frequently lethal. 1'7"8'~3'~8'25Several studies have shown an increased incidence of sudden death in achondroplastic dwarfs under 4 years of age. ~'8"~7In these studies, the increased mortality in this age group has been attributed directly to acute compression of the brain stem and upper cervical cord. Hecht, et al., 8 calculated a 7.5% risk of sudden death in achondroplastic patients during the 1st year of life, a risk calculated to be at least three times greater than that of the general population. 17 Craniocervical Decompression Given this relatively bleak picture, several centers have performed craniocervical decompression on achondroplastic infants with cervicomedullary compression, generally obtaining good results. 6'~3'~8'24 Frequent screening of young patients with achondroplasia for respiratory and neurological impairment and performing early decompression in cases of proven cervicomedullary compression have therefore been recommended. 6'~8'24 Unfortunately, the small numbers of surgical patients in these studies and the lack of follow-up data over a longer period have not allowed a more definitive assessment of the efficacy of this treatment in individuals with heterozygous achondroplasia. Evidence supporting surgical intervention in patients with homozygous achondroplasia is even scantier. ~4 The present study, although necessarily limited by its retrospective nature, provides data by which to evaluate the efficacy of craniocervical decompression in young achondroplastic patients with cervicomedullary compression. As our results indicate, decompression of the cervicomedullary junction in these patients will often bring about a dramatic and sustained improvement in neurological and respiratory function. No patient in our
379
J. Aryanpur, et al. series suffered a decline in neurological status following the procedure. All patients who presented with primarily motor findings were improved postoperatively. Rapid attainment of motor milestones and resolution of hyperreflexia and hypertonia were common. Apnea or cyanosis was a common presenting problem and was corrected in six of the eight patients so afflicted by craniocervical decompression. The remaining two patients improved following surgery directed toward coexistent obstructive respiratory problems. Thus, craniocervical decompression is an effective treatment for cervicomedullary compression in young patients with achondroplasia.
Respiratory Compromise A previous studyTM has reported a 35% incidence of respiratory difficulties in pediatric achondroplastic patients. In some of these patients, respiratory abnormalities were not suspected by referring physicians or parents, and were only detected after workup for unrelated problems. Our results confirm that respiratory dysfunction is a common problem in pediatric achondroplastic patients, and one which may indicate ongoing brainstem compression. In achondroplastic patients, respiratory compromise may be caused by any of several different mechanisms. Purely obstructive etiologies, including upper airway obstruction secondary to micrognathia, facial and laryngeal hypoplasia, and hypotonia of laryngeal musculature, are common. 11,18.22Restrictive pulmonary disease caused by thoracic cage and chest wall deformities may also contribute to respiratory compromise. 18'2z Compression of brain-stem respiratory centers by a small foramen magnum can interfere with central respiratory drive, causing central apnea. 6'~7'18.22In addition, compression of the brain stem and upper cervical cord may directly compress the lower motor neuron systems controlling respiratory muscles, resulting in weak, ineffective respirations. 8"22 Because primary and neurogenic causes of respiratory dysfunction may coexist in the same patient, differentiation between these forms of respiratory compromise is important but often difficult. Patients with primarily obstructive or restrictive pulmonary disease would not be expected to benefit from craniocervical decompression. Conversely, apnea of central origin would not be improved by efforts directed toward a coexistent but minor obstructive component. One of our patients had undergone tracheostomy prior to craniocervical decompression without relief of respiratory difficulties. Two of our patients with cervicomedullary compression required tracheostomy or tonsillectomy and adenoidectomy subsequent to craniocervical decompression because of concomitant obstructive respiratory compromise. Thus, treatment of both obstructive and central apnea may be necessary in this group of patients. Our experience suggests that the coordinated efforts of experienced pediatricians, neurologists, neurosurgeons, radiologists, otolaryngologists, and pulmonologists are vital in deter380
mining which achondroplastic children may benefit from foramen magnum decompression.
Motor Deficits Although the most dangerous consequence of cervicomedullary compression is respiratory arrest via mechanisms described above, other neurological deficits may result from compression of descending and ascending white matter tracts. Hypertonia, upper- and lower-extremity weakness, and spasticity have all been described. 7'13'24'25 Long-standing compression may result in irreversible spinal cord changes and a fixed deficit. 7'25 For this reason, early decompression is recommended in all proven cases of cervicomedullary compression. Pathogenesis of Foramen Magnum Stenosis The pathogenesis of foramen magnum stenosis in achondroplastic patients appears to be related to the generalized defect in endochondral bone formation. ~3 This results in an abnormally small posterior fossa with an extremely horizontally oriented posterior rim. Typically, the posterior lip of the foramen magnum itself is thickened and indents the cervicomedullaryjunction. In addition, a thick band of connective tissue often constricts the theca further at the foramen magnum. Wang, et al.,23 and Hecht, et al.,9 have studied the CT appearance of craniocervical junction abnormalities in pediatric achondroplastic patients. A small, teardropshaped foramen magnum was characteristic. In the study by Wang, et al., 96% of patients evaluated had sagittal and coronal foramen magnum dimensions at least 3 standard deviation smaller than those of agematched control individuals. Surgical Decompression Relief of cervicomedullary compression requires removal of both the osseous and soft-tissue constrictive elements. The use of the high-speed drill provides for rapid controlled removal of bone around the cervicomedullary junction, and should be considered an essential part of the procedure. Removal of bone alone is in general not sufficient to relieve the compression, however. In many cases the release of thick dural constricting bands was required to allow free CSF flow and pulsation around the brain stem and upper cervical cord. Since it is difficult to evaluate the degree of dural impingement upon the cervicomedullary junction by simple inspection, we recommend that the dura be opened in all cases and that patch duroplasty be performed when dural constriction exists. Cerebrospinal Fluid Dynamics Unfortunately, the dural opening required to achieve adequate decompression was also the cause of the major early morbidity associated with this procedure, namely CSF leakage from the surgical wound. Despite meticulous attention to the dural closure techniques, two patients developed postoperative CSF leakage from the suboccipital incision. Under ordinary circumstances a J. Neurosurg. / Volume 73/September, 1990
Craniocervical decompression in achondroplasia properly closed dural suture line would be expected to be watertight; however, it is well recognized that, in achondroplastic patients, CSF dynamics are often abnormal. ~5'2~'24In these patients, ventriculomegaly, abnormally capacious subarachnoid spaces over the cerebral convexities, elevated ICP, and even frank hydrocephalus may' be observed. 15"2~-24 The etiology of the abnormal CSF dynamics associated with achondroplasia is not clear; however, recent work points to stenosis of skull outlet foramina and consequent increased jugular and intracranial venous pressures as a prime causative factor. 21 In the achondroplastic patient with ventriculomegaly but without clear-cut symptomatic hydrocephalus, ventricular shunting is probably best avoided as evidence exists that the condition is not progressive in most patients. 3"24Unfortunately, a significant percentage of achondroplastic patients will eventually develop symptomatic hydrocephalus and require a shunting procedure, At least nine of the 15 patients in the present study had evidence of ventriculomegaly on CT scans or MR images, and four eventually underwent shunt placement. Ventriculomegaly alone need not signi~ Tactive hydrocephalus: however, it probably does indicate a common underlying abnormality of CSF dynamics which, in some patients, may progress to symptomatic hydrocephalus. The high incidence of postoperative CSF leakage from the suboccipital wound in the early cases in this series probably reflected the tendency toward elevated ICP in these patients. Undoubtedly, the inherent friability of pediatric skin and subcutaneous tissues further compounded the problem by providing a weak barrier against elevated CSF pressures. The institution of controlled perioperative CSF diversion via ventriculostomy in the later patients in this series dramatically reduced the incidence of suboccipital wound CSF leakage. In an analogous situation, shunt placement in the newborn with hydrocephalus and a repaired myelomeningocele protects the myelomeningocele wound. Development of CSF leakage from the EVD site itself in two later patients further underscores the existence of abnormal CSF dynamics in patients with achondroplasia, as we have not encountered this problem in individuals with normal CSF dynamics. In addition to CSF diversion, the ability to monitor ICP postoperatively may yield information important in determining which patients might ultimately need shunt placement. Thus, the benefits of perioperative ventriculostomy appear to outweigh the risks associated with the procedure in this group of patients. Conclusions
The treatment of pediatric achondroptastic patients is challenging and requires a coordinated multidisciplinary approach. Although a condition not frequently encountered, the high incidence of compression of the neuraxis and its dangerous sequelae in this patient population mandate familiarity with the available therJ. Neurosurg. / Volume 73/September, 1990
apies. In documented cases of cervicomedullary compression in pediatric achondroplastic patients, early surgical decompression utilizing the techniques described above appears to improve significantly the natural history of this condition. References
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8. Hecht JT, Francomano CA, Horton WA, et al: Mortality in achondroplasia. Am J Hum Genet 41:454-464, 1987 9. Hecht JT, Nelson FW, Butler IJ, et al: Computerized tomography of the foramen magnum: achondroplastic values compared to normal standards. Am J Med Genet 20:355-360, 1985 10. Heinz ER, Ward A, Drayer BP, et al: Distinction between obstructive and atrophic dilatation of ventricles in children. J Comput Assist Tomogr 4:320-325, 1980 I 1. Larsen PD, Synder EW, Matsuo F, et al: Achondroplasia associated with obstructive sleep apnea. Arch Neurol 40:769, 1983 (Letter) 12. Lutter LD, Langer LO: Neurological symptoms in achondroplastic dwarfs - - surgical treatment. J Bone Joint Surg (Am) 59:87-92, 1977 13. Luyendijk W, Matricali B, Thomeer RTWM: Basilar impression in an achondroplastic dwarf: causative role in tetraparesis. Acta Neurochir 41:243-253, 1978 14. Moskowitz N, Carson B, Kopits S, et al: Foramen magnum decompression in an infant with homozygous achondroplasia. Case report. J Neurosurg 70:t26-128, 1989 15. Mueller SM, Bell W, Cornell S, et al: Achondroplasia and hydrocephalus. Neurology 27:430-434, 1977 16. Oberklaid F, Danks DM, Jensen F, et al: Achondroplasia and hydrochondroplasia. Comments on frequency, mutation rate, and radiological features in skull and spine. J Med Genet 16:140-146, 1979 17. Pauli RM, Scott CI, Wassman ER Jr, et al: Apnea and sudden unexpected death in infants with achondroplasia. J Pediatr 104:342-348, 1984 18. Reid CS, Pyeritz RE, Kopits SE, et al: Cervicomedullary compression in young patients with achondroplasia: value of comprehensive neurologic and respiratory evaluation. J Pediatr 110:522-530, 1987 19. Shikata J, Yamamuro T, Iida H, et al: Surgical treatment of achondroplastic dwarfs with paraplegia. Surg Neurol 381
J. Aryanpur, et al. 29:125-130, 1988 20. Spillane JD: Three cases of achondroplasia with neurological complications. J Neurol Neurosurg Psychiatry 15: 246-252, 1952 21. Steinbok P, Halt J, Flodmark O: Hydrocephalus in achondroplasia: the possible role of intracranial venous hypertension. J Neurosurg 71:42-48, 1989 22. Stokes DC, Phillips JA, Leonard CO, et al: Respiratory complications of achondroplasia. J Pediatr 102: 534-541, 1983 23. Wang H, Rosenbaum AE, Reid CS, et al: Pediatric patients with achondroplasia: CT evaluation of the craniocervical junction. Radiology 164:515-519, 1987 24. Yamada H, Nakamura S, Tajima M, et al: Neurological manifestations of pediatric achondroplasia. J Neurosurg 54:49-57, 1981
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Manuscript received November I, 1989. Accepted in final form February 5, 1990. Address reprint requests to." John Aryanpur, M.D., Department of Neurosurgery, Meyer 7-109, The Johns Hopkins Hospital, 600 North Wolfe Street, Baltimore, Maryland 21205.
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