Keywords
craniocervical junction osteomyelitis - endoscopic transnasal odontoidectomy - extended
endonasal approach - spine infection - skull base - C1 - odontoid - dens
Introduction
Pyogenic osteomyelitis of the craniocervical junction is a rare event that has been
infrequently described in the literature.[1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9] The clinical manifestations most often include neck pain, stiffness, swelling, and
dysphagia, although this entity may also present with meningitis. Most commonly afflicted
are elderly or immunocompromised patients harboring comorbidities such as diabetes
or end-stage renal disease. In the setting of sepsis despite the use of broad-spectrum
intravenous antibiotics, surgical debridement of infected vertebral bone may be required.
In addition, ventral spinal cord impingement with atlantoaxial instability, fluid
accumulation, and bony degeneration from septic arthritis may develop acutely, requiring
urgent decompression. Surgical decompression of this site has traditionally been performed
via the transoral approach.[2]
[10]
[11] However, this technique is often associated with notable morbidities, including
velopharyngeal insufficiency, postoperative dysphagia, and surgical bed contamination
from saliva, oral flora, and food particles in the presence of active cervical spine
infection. As such, the transoral approach can be particularly challenging for immunocompromised
patients with poor baseline health status. We and others more recently described the
transnasal endoscopic approach to the craniocervical junction including endoscopic
transnasal odontoidectomy.[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24] To date, the application of this advanced procedure has remained limited to a few
specialized academic surgical centers. However, the feasibility of this approach has
been demonstrated in the treatment of atlantoaxial subluxation, rheumatoid pannus,
and other mass lesions producing ventral medullary compression. Importantly, this
approach is amenable to complete resection of the odontoid process, and has thus far
been associated with highly favorable clinical outcomes. Management of cerebrospinal
fluid (CSF) leak at the craniocervical junction, where primary dural repair is not
possible, also represents a reconstructive challenge for this remote skull base defect,
which may itself contribute to secondary brainstem compression. We present two cases
utilizing the transnasal endoscopic approach for treatment of acute craniocervical
junction osteomyelitis at the in the setting of frank immunosuppression. We further
discuss methods for successful endoscopic repair of challenging CSF leaks in this
rare location of the ventral skull base.
Case 1
History
A 69-year-old female patient with a medical history, including rheumatoid arthritis
initially presented to her primary care provider with 3 weeks of progressive neck
pain and upper/lower extremity paresis. Magnetic resonance imaging (MRI) revealed
a dense C1/C2 pannus with invagination of the thecal sac. After 1 day, she was admitted
to a local hospital with altered mental status where further questioning revealed
a history of low-grade fever and chills, odynophagia, diplopia, blurry vision, and
photophobia. Upon transfer to our tertiary care institution, the patient's physical
examination was notable for a right third nerve palsy, dense hemiparesis in the left
upper and lower extremities, and fluctuating mental status with intermittent unresponsiveness.
Laboratory values on admission demonstrated marked leukocytosis in both blood and
CSF specimens and elevated inflammatory markers. Brain and cervical spine MRI revealed
cerebritis, intraventricular regions of diffusion restriction indicative of purulence,
and an enhancing collection at the atlantoaxial junction resulting in compression
of the ventral spinal cord. Empiric intravenous antibiotics were initiated and blood
cultures ultimately grew Streptococcus pneumoniae. The patient was initially deemed too unstable to undergo transoral decompression
of the craniocervical junction, although her mental status gradually improved with
antibiotics. Her left arm and leg weakness persisted and repeat MRI 5 days later redemonstrated
an enhancing collection at the atlantoaxial junction concerning for epidural abscess
with severe canal stenosis and intrinsic cervicomedullary cord-signal change ([Fig. 1A, B]). A computed tomography (CT) scan demonstrated bony reaction and neo-osteogenesis
at C1/2 ([Fig. 1C]) suggestive of vertebral osteomyelitis. In light of an improvement in mental status,
we elected to pursue transnasal surgical debridement and decompression of the craniocervical
junction.
Fig. 1 Case 1: (A) Gadolinium enhancement posterior to the dens is seen with significant
mass effect on the cevicomedullary junction. (B) Signal abnormality is seen in the
upper cervical cord and medulla as well as bone on T2-weighted MRI. (C) Preoperative
CT angiogram highlights bony changes, vascular structures (arrows), and unobstructed
access to the atlantoaxial junction via the endonasal route. (D) C1–2 posterior instrumentation
is seen on lateral X-ray. (E) Postoperative CT demonstrates the extent of bony resection
achieved (arrows). (F) Postoperative T2-weighted MRI confirms decompression of the
cervicomedullary junction. CT, computed tomography; MRI, magnetic resonance imaging.
Intervention
Preoperative CT scan utilizing the hard palate suggested appropriately achieved surgical
access via transnasal approach. CT angiography ([Fig. 1C]) documented the course of the vertebrobasilar arteries and the hypoglossal canals
for intraoperative navigation following posterior cervical fusion (see [Fig. 1D]). After 2 days, an anterior transnasal debridement was performed as a combined procedure
between neurosurgery and otolaryngology. After upfront placement of a lumbar drain,
the transnasal approach included bilateral inferior turbinate outfractures and a posteroinferior
septectomy. After adequate nasopharyngeal soft tissue removal, access to the posterior
fossa skull base and atlantoaxial joint was obtained. Extended diamond bits were used
to widely drill down the anterior arch of C1 from a lateral-to-medial direction, using
intraoperative image guidance to confirm the course of the vertebral arteries. Abnormal
fibrous and seemingly infected granulation tissue was noted within the C1 and C2 joint
space that was subsequently resected. Following this, a diseased odontoid process
was found to be associated with significant scarring and firmly adherent to the dura
overlying the basilar cistern. Extensive drilling at the base of the odontoid process
permitted anterior displacement and removal of the dens.
Although successful decompression was achieved, a 1.5 cm dural tear was clearly noted
at the site of odontoid–dural tethering and displacement, leading to frank CSF drainage
and ballooning of the dura ventrally into the surgical field. This provided a challenge
given the remote surgical corridor of 13 to 14 cm posterior to the nostril rim, and
the need to avoid brainstem compression in the process of bolstering a dural repair
construct. We elected to proceed with a multilayered onlay technique, reserving the
option of a nasoseptal flap for the setting of persistent fistula. DuraGen matrix
(Integra LifeSciences Corp., Plainsboro Township, New Jersey, United States) was placed
atop the dural defect, followed by abdominal fat graft placement, and Tisseel (Baxter
Healthcare Corp., Illinois, Deerfield, United States). To close the sizeable dead
space within the endoscopic corridor, a second layering consisting of fat, Gelfoam
(Pfizer Corp., New York, New York, United States) and Tisseel was utilized. For final
support of the reconstruction, resorbable Nasopore (Polyganics Corp., Groningen, The
Netherlands) microfibrillar sponge was partially extended into the reconstruction,
spanning across the soft palate, and onto the nasal floor. No evidence of CSF leak
was detected upon multiple Valsalva maneuvers and lumbar CSF diversion was maintained
at 15 mL/h.
The patient was extubated, and tolerated an oral diet on postoperative day 1. Postoperative
imaging demonstrated complete anterior resection of C1 and C2 with brainstem decompression
without evidence of secondary compression following reinforcement of the multilayered
reconstruction ([Fig. 1E, F]). Coagulase-negative Staphylococcus grew from intraoperative cultures to direct future parenteral antibiotics. The patient
was discharged on postoperative day 5 following discontinuation of CSF diversion.
Follow-Up
The patient made steady neurologic recovery without noting postoperative rhinorrhea,
velopharyngeal insufficiency, or Eustachian tube dysfunction at any time. Endoscopic
visualization of the surgical site 3 months postoperatively revealed a completely
remucosalized nasopharynx without any gross evidence of surgical manipulation. Follow-up
neurological examination 6 months after the surgery revealed 5/5 strength in the previously
weak upper extremity; no meningeal signs or rhinorrhea were present, and the posterior
cervical incision was well healed. By this time the patient had returned to work as
an administrative assistant.
Case 2
History
A 55-year-old male patient was transferred to our institution with progressive headaches,
a “clicking, unstable” sensation in his neck, and a large, enhancing ventral epidural
collection was noted to be impinging the cervicomedullary junction. His medical history
included diabetes mellitus, hypertension, hyperlipidemia, and intravenous drug abuse.
Few years ago, he had undergone a prior C3–C7 anterior fusion with C3–4 cage placement
and C3–T1 posterior stabilization at an outside hospital for cervical spondylosis,
he had a persistent C3–4 myelomalacia and walked with a cane at baseline. Upon transfer,
the patient was afebrile and cognitively intact with no meningeal signs or focal weakness,
though he had immunosuppression secondary to poorly controlled diabetes in the setting
of intravenous (IV) drug use. Laboratory workup revealed elevated inflammatory markers,
but no leukocytosis. Empiric broad-spectrum antibiotics were initiated. Preoperative
MRI demonstrated a large, heterogeneously enhancing collection at the atlantoaxial
articulation with effacement of the thecal sac ([Fig. 2A, B]). Additional imaging findings included bony thickening and neo-osteogenesis of the
anterior arch of C1, the body of C2, and the base of the odontoid process ([Fig. 2C]). Anterior and posterior instrumentation was present from C3–T1 with good bony fusion.
In view of the patient's progressive symptoms, large enhancing cervicomedullary collection
and relatively stable medical condition, he was deemed an appropriate candidate for
surgical decompression.
Fig. 2 Case 2: (A) Preoperative T1-weighted imaging with gadolinium demonstrates an enhancing
collection centered at the atlantoaxial junction. (B) T2-weighted imaging shows heterogeneous
signal intensity in the collection with posterior mass effect. (C) Coronal (upper
panel), and axial (lower panel) CT cuts through the atlantoaxial joint suggestive
of diseased bone. (D) Lateral X-ray demonstrating extension of the previous construct
to the occiput. Also visible is the patient's previous anterior fusion. (E) Intraoperative
CT confirming the extent of odontoid resection. (F) Postoperative T1-weighted image
with gadolinium after resection demonstrating cervicomedullary decompression. CT,
computed tomography.
Intervention
Preoperative CT imaging confirmed the presence of an adequate surgical corridor to
the atlantoaxial junction via a transnasal approach. As such, a two-stage operation
was planned to treat the presumed atlantoaxial osteomyelitis. Initial posterior stabilization
was first extended to the occiput ([Fig. 2D]). Two days later, after lumbar drain placement and setup of intraoperative navigation,
a multidisciplinary anterior debridement was performed with computer-assisted stereotactic
navigation as a joint operation involving otolaryngology and neurosurgery in a similar
fashion to Case 1. Red rubber catheters were utilized for intermittent soft palate
retraction. Curved and extended 3- and 4-mm coarse diamond drill bits were used to
take down the arch of C1 and inferior aspect of the clivus exposing thick granulation
tissue. Additional fibrotic inflammatory tissue and soft tissue edema were noted in
the C1–C2 region, but no frank purulence was appreciated. Successful dural decompression
was confirmed endoscopically and corroborated with intraoperative CT ([Fig. 2E]). Although no CSF was seen, a dural defect was noted with exposed arachnoid. As
such, an abdominal fat graft was placed against the dura along with Gelfoam and Tisseel.
The indwelling lumbar drain was placed to drain at 15 mL/h given the possibility of
CSF leak from the basilar cistern. The patient was slow to wean off of the ventilator,
but was extubated uneventfully on postoperative day 3. Postsurgical imaging confirmed
optimal decompression of the cervicomedullary junction ([Fig. 2F]). Pathology demonstrated granulation tissue and inflamed synovium, but interestingly
all cultures remained negative throughout his hospital course, likely due to concurrent
use of intravenous antibiotics during surgery. After consulting with the infectious
disease team, antibiotics were discontinued and the patient was discharged home on
postoperative day 7.
Follow-Up
At 3-month follow-up, the patient reported complete resolution of his preoperative
symptoms, denied any new symptoms of velopharyngeal insufficiency, Eustachian tube
dysfunction, and his neurological examination was only notable for the new limited
cervical range of motion consistent with occipitocervical fusion. On examination,
the posterior cervical incision was well healed and his nasal endoscopy showed a widely
remucosalized nasopharynx without pooling of secretions or edema.
Discussion
Vertebral osteomyelitis comprises only 2 to 4% of all cases of osteomyelitis and involvement
of the craniocervical junction represents an especially rare subset of this acute
inflammatory disease process. CSF fistula occurring in the setting of osteomyelitis
is also quite atypical, but must be recognized in a timely manner—particularly in
patients presenting with meningitis and/or immunosuppression. In this setting, Staphylococcus aureus is recognized as the most common causative microorganism[2] although infection with Streptococcus
[9] and gram-negative organisms has been reported. As illustrated in this case series,
notable risk factors for acute skull base osteomyelitis include diabetes mellitus,
intravenous drug abuse, active immunosuppression, and hemodialysis.[9]
Although IV antibiotics can successfully treat this dire condition, in selected cases,
acute surgical decompression may be required in cases of infected and degenerated
vertebral bone causing cervicomedullary compression. Transoral decompression has been
the “gold standard” procedure for anterior decompression of C1 and C2, however, there
may be disadvantages to this approach, specifically in the setting of acute osteomyelitis,
and immunocompromised with poor baseline health.[1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9] These include a long surgical corridor with limited visualization, and limited manual/digital
access beyond the oral cavity given dental, occlusal, and palatal anatomic constraints.
Following a transoral approach, there is exposure of the surgical bed to saliva and
oral contents with each swallow raising concern for impaired healing or infection,
especially in the event of CSF leakage. Postoperative oropharyngeal swelling increases
the concern for safe extubation, and often dictates consideration of tracheostomy
and feeding tube placement. These concerns are again naturally exacerbated in immunocompromised
patients with poor baseline health, as is frequently the case in those presenting
with craniocervical osteomyelitis and ventral epidural abscess.
We and others have previously described the transnasal approach to the craniocervical
junction for several etiologies.[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24] Advantages to the transnasal approach include outstanding endoscopic visualization
of the full length of the deep surgical corridor created, favorable nasal mucosal
wound healing, early advancement to an oral diet, and the reduced likelihood of prolonged
postoperative intubation due to concerns of surgical site swelling. Disadvantages
are primarily (1) anatomic, as the hard palate of the oral cavity limits endoscopic
instrumentation below the C2 vertebral body, and (2) technical, given the need for
multidisciplinary surgical expertise with endonasal neurosurgery and for specialized
equipment required to access this distant skull base location. In addition to acute
skull base osteomyelitis, we have previously also utilized the transnasal approach
for decompression of patients with cervicomedullary tumor, rheumatoid arthritis, and
degenerative pseudotumor.[14]
[19] Postoperatively, both patients detailed herein were extubated and tolerated an oral
diet 1 to 3 days after surgery, which may not be feasible until several days after
a transoral approach.
Careful judgment must be employed in determining when transnasal versus transoral
decompression is appropriate. Anatomic considerations were recently highlighted by
the Rhoton group who compared the two approaches in 10 cadaveric specimens and proposed
use of a combined approach when necessary.[20] Following cervical fusion, our evaluation begins with a thin-cut CT scan and angiogram
of the nasal cavity and craniocervical junction to fully delineate all critical neurovascular
anatomy, and to ascertain whether the hard palate will markedly restrict inferior
access to C2 ([Fig. 1D]). In all cases, there will be bony deformation at the skull base, and important
surgical landmarks, such as, the C1 tubercle may in fact be eroded, increasing the
risk of inadvertent vertebral artery injury. We consistently utilize intraoperative
stereotactic navigation with merged stereotactic MRI and CT angiogram sequences to
attain reliable positional verification to mitigate this risk.[14]
Both of our patients were treated in a staged fashion with initial posterior stabilization.
We are strong advocates that posterior stabilization should precede all considerations
of anterior endonasal surgery. Arthrodesis at C1/2 was adequate for the first case.
For the second patient, osteomyelitis involving the C1 lateral masses in conjunction
with the patient's preexisting instrumentation necessitated extension of fixation
to the occiput. Two days following the posterior stabilization, we utilized a transnasal
approach for mandatory urgent debridement of diseased bone and infected tissue, achieving
both decompression, surgical clearance of frankly diseased tissue, infection and inflammation,
and pathologic diagnosis.
A large 1 cm dural tear occurred after successful decompression during the first case,
and exposed arachnoid was visualized in the second case suggestive of elevated risk
for postoperative CSF leakage despite no visualization of CSF. Although primary dural
repair in the premedullary space is challenging, we successfully reconstructed even
the 1-cm defect using a multilayered onlay grafting technique consisting of DuraGen
sheeting, abdominal fat, Gelfoam, fibrin glue, and biosorbable polyurethane sponge
(Nasopore). Importantly, this reconstruction of the surgical defect did not produce
secondary brainstem compression, and obviated the need for pedicled intranasal flap
maneuvers.
Both patients had lumbar drains placed at the outset of each case, in anticipation
of the need for CSF diversion following endonasal surgery in these acutely infected/inflamed
surgical beds. Strategically, early lumbar drain placement at case start is readily
performed, and obviates the need to reposition the patient in a lateral decubitus
position after insetting a multilayered reconstruction. Our experience and that of
others[25] suggests that a drainage rate of at least 15 mL/h may be required in some cases
to alleviate CSF leakage. Clinical judgment must be used to weigh the risks of postoperative
CSF leakage against those incurred by CSF diversion. In these immunocompromised patients
with likely suboptimal wound healing and dural defects in the premedullary space,
we felt that drainage at 15 mL/h was warranted. Although no adverse effects were observed
in either patient, use of a lumbar drain requires vigilant monitoring for symptoms
of intracranial hypotension, including depressed consciousness, especially when higher
drainage rates are employed.[26]
[27]
In summary, this case series details the successful use of endoscopic transnasal anterior
decompression to treat basilar invagination secondary to acute skull base osteomyelitis,
and adds to the growing literature in support of the transnasal endoscopic approach
as a safe and feasible means for decompressing the craniocervical junction, now also
in the setting of active infection and inflammation in immunocompromised patients.
Judicious patient selection, combined with sound clinical judgment, access to instrumentation
and intraoperative imaging cannot be overemphasized. CSF leaks at this distant location
anterior to the brainstem can also be successfully repaired with bolstered multilayered
reconstructive materials without secondary neurologic consequences or impeding the
goal of decompressing the ventral posterior fossa skull base.
