The suboccipital ligament

View More View Less
  • 1 College of Medicine and
  • 2 Department of Neurosurgery, University of Tennessee Health Science Center;
  • 3 Pathology Group of the Midsouth;
  • 4 American Esoteric Laboratories;
  • 5 Semmes-Murphey Clinic, Memphis, Tennessee; and
  • 6 Department of Neurosurgery, Osijek University School of Medicine, Osijek, Croatia
Full access

OBJECTIVE

A fibrous structure located dorsal to the dura at the posterior craniocervical junction stretches horizontally between the bilateral occipital condyles and the upper borders of the C-1 laminae. Partially covered by the occipital bone, this structure is always encountered when the bone is removed from the foramen magnum rim during approaches to the posterior cranial fossa. Although known to surgeons, this structure has not been defined, studied, or named. The most appropriate name for this structure is “the suboccipital ligament,” and a detailed rationale for this name is provided.

METHODS

This 3-year-long study included 10 cadaveric specimens and 39 clinical patients: 31 consecutive surgically treated patients with Chiari Type I malformations (CM-I subgroup) and 8 other patients with posterior fossa pathologies (non–CM-I subgroup). The dimensions were defined, the function of this ligament was hypothesized, size and histological composition were compared between patient subgroups, and its origin and relationship to the surrounding structures were analyzed. Possible statistical differences in the parameters between the 2 groups were also evaluated.

RESULTS

The suboccipital ligament consists of horizontally oriented hyaline fibers and has a median length of 35 mm, height of 10 mm, and thickness of 0.5 mm. These dimensions are not significantly different between the CM-I and non–CM-I patients. The median age of the patients was 43 years, with CM-I patients being significantly younger (median 35 years) than non–CM-I patients (median 57 years). There was no statistically significant difference in weight, height, and body mass index between patient subgroups. There was no significant correlation between the body mass index or height of the patients and the dimensions of the ligament. No statistically significant differences existed between the subgroups in terms of smoking history, alcohol consumption, and the presence of diabetes mellitus, hypertension, hydrocephalus, or headaches. The ligament tissue in the CM-I patients was disorganized with poorly arranged collagen bands and interspersed adipose tissue. These patients also had more hyalinized fibrosis and showed changes in the direction of fibers, with hyaline nodules ranging from 0 to 2+. The result of the histological evaluation of the suboccipital ligament for hyaline nodules, calcification, and ossification was graded as 2+ if present in 3 or more medium-power magnification fields (MPFs); 1+ if present in 1–2 MPFs; and 0, if present in less than 1 MPF. Histological examination of the ligaments showed structural differences between CM-I and non–CM-I patients, most notably the presence of hyaline nodules and an altered fiber orientation in CM-I patients.

CONCLUSIONS

The suboccipital ligament extends between the occipital condyle and the superior edge of the C-1 lamina, connecting the contralateral sides, and appears to function as a real ligament. It is ventral to the occipital bone, which covers approximately two-thirds of the height of the ligament and is loosely attached to the dura medially and more firmly laterally. Because of its distinctive anatomy, characteristics, and function, the suboccipital ligament deserves its own uniform designation and name.

ABBREVIATIONS BMI = body mass index; CM-I = Chiari malformation Type I; MPF = medium-power magnification field.

OBJECTIVE

A fibrous structure located dorsal to the dura at the posterior craniocervical junction stretches horizontally between the bilateral occipital condyles and the upper borders of the C-1 laminae. Partially covered by the occipital bone, this structure is always encountered when the bone is removed from the foramen magnum rim during approaches to the posterior cranial fossa. Although known to surgeons, this structure has not been defined, studied, or named. The most appropriate name for this structure is “the suboccipital ligament,” and a detailed rationale for this name is provided.

METHODS

This 3-year-long study included 10 cadaveric specimens and 39 clinical patients: 31 consecutive surgically treated patients with Chiari Type I malformations (CM-I subgroup) and 8 other patients with posterior fossa pathologies (non–CM-I subgroup). The dimensions were defined, the function of this ligament was hypothesized, size and histological composition were compared between patient subgroups, and its origin and relationship to the surrounding structures were analyzed. Possible statistical differences in the parameters between the 2 groups were also evaluated.

RESULTS

The suboccipital ligament consists of horizontally oriented hyaline fibers and has a median length of 35 mm, height of 10 mm, and thickness of 0.5 mm. These dimensions are not significantly different between the CM-I and non–CM-I patients. The median age of the patients was 43 years, with CM-I patients being significantly younger (median 35 years) than non–CM-I patients (median 57 years). There was no statistically significant difference in weight, height, and body mass index between patient subgroups. There was no significant correlation between the body mass index or height of the patients and the dimensions of the ligament. No statistically significant differences existed between the subgroups in terms of smoking history, alcohol consumption, and the presence of diabetes mellitus, hypertension, hydrocephalus, or headaches. The ligament tissue in the CM-I patients was disorganized with poorly arranged collagen bands and interspersed adipose tissue. These patients also had more hyalinized fibrosis and showed changes in the direction of fibers, with hyaline nodules ranging from 0 to 2+. The result of the histological evaluation of the suboccipital ligament for hyaline nodules, calcification, and ossification was graded as 2+ if present in 3 or more medium-power magnification fields (MPFs); 1+ if present in 1–2 MPFs; and 0, if present in less than 1 MPF. Histological examination of the ligaments showed structural differences between CM-I and non–CM-I patients, most notably the presence of hyaline nodules and an altered fiber orientation in CM-I patients.

CONCLUSIONS

The suboccipital ligament extends between the occipital condyle and the superior edge of the C-1 lamina, connecting the contralateral sides, and appears to function as a real ligament. It is ventral to the occipital bone, which covers approximately two-thirds of the height of the ligament and is loosely attached to the dura medially and more firmly laterally. Because of its distinctive anatomy, characteristics, and function, the suboccipital ligament deserves its own uniform designation and name.

ABBREVIATIONS BMI = body mass index; CM-I = Chiari malformation Type I; MPF = medium-power magnification field.

There is a fibrous structure located dorsal to the dura at the posterior craniocervical junction that stretches horizontally between the bilateral occipital condyles and the upper borders of the C-1 laminae. It is partially covered by the occipital bone. This structure is always encountered when the occipital bone is removed from the foramen magnum rim during approaches to the posterior cranial fossa to decompress a Chiari Type I malformation (CM-I), resect a cerebellar tumor, or address other surgical pathologies.

Although known to surgeons who operate in this area, this structure has not been precisely defined, systematically studied, or even acceptably and universally named. In the neurosurgical literature, it has been sporadically mentioned as a “dural band,”1,2,6,10,14,16,18,25,27,30,32,38,40–42 “band of dura,”28,29 “thickened dura mater,”9,12 “fibrous band,”11,24,33 “posterior atlanto-occipital ligament,”15 “atlanto-occipital membrane,”21 “fibrodural band,”22 “thick band,”23 “epidural fibrosis,”35 “dense constrictive band,”36 and “thickened posterior atlanto-occipital membrane dural band.”37

Surprisingly, there is no mention of this structure in Gray's Anatomy20 or other anatomy atlases or books. Furthermore, its histological composition is unclear and it is unknown whether this ligament plays any role in the pathology of CM-I or is associated with the formation or extent of syrinx. It is also unknown whether there is any difference in ligament size (width, height, thickness) or histological structure in patients with different posterior cranial fossa pathologies, whether there is any difference in its characteristics between males and females, or if there are any differences in this ligament among patients with congenital, degenerative, or neoplastic processes.

We have studied this structure in cadaveric specimens and clinically, and we compared its size and histological composition in a series of CM-I patients and patients with various posterior cranial fossa pathologies. We believe that the most appropriate name for this structure is the “suboccipital ligament” and provide a detailed rationale for this name. We have analyzed its origin, its relationship with the posterior suboccipital membrane, the occipital bone, and the dura, and hypothesized its function. Furthermore, we have measured its various dimensions, analyzed it histologically, and carried out numerous comparisons of its various properties and tested them statistically.

Methods

This prospective anatomical and clinical study was approved by the appropriate hospital institutional review board (Semmes-Murphy Clinic/Baptist Memorial Hospital). It was conducted over a 3-year period (February 2012 to February 2015). Our study included 10 cadaveric specimens and, subsequently, 39 clinical patients: 31 consecutive surgically treated patients with CM-I (CM-I subgroup) and 8 additional patients with other posterior fossa pathologies (non–CM-I subgroup). All patients were operated on by the senior author (K.I.A.).

Surgical Approach

We began this study with cadaveric specimens. Once we defined the details of the ligament's anatomy, origins, and relationships, we initiated the clinical study. For the approach, a midline skin incision was made, extending from the external occipital protuberance to the C-2 spinous process. The incision was carried down through the nuchal ligament in the midline using Bovie cautery. The suboccipital muscles were then dissected and retracted laterally with self-retaining curved cerebellar retractors, and the posterior atlantooccipital membrane was resected sharply from the occipital bone and C-1 lamina. The posterior lamina of C-1 was then resected approximately 2 cm wide with the C-1 attachment for the Midas Rex drill (Medtronic). Subsequently, with a 6-mm coarse diamond tip drill, we created a gutter in the bone that extended laterally just medial to the occipital condyles and superior to the area between superior and inferior nuchal lines. The inner table of the bone in the gutter created by drilling was resected using 2-mm Kerrison rongeurs. The dura overlying the posterior cranial fossa was reached ventrally at the drilled-out bone groove without violation. The free craniectomy piece was thus created and freed from the rest of the occipital bone. Semioval in shape, it was then sharply elevated, keeping the suboccipital ligament intact. Any bleeding was easily controlled with Gelfoam powder (Pfizer). The surgical field was irrigated with antibiotic saline and evacuated with suction to eliminate any bone dust created by drilling. This was done to prevent false-positive results of calcification and ossification foci in the suboccipital ligament.

The suboccipital ligament was then studied intraoperatively, including its anatomical features such as its origins, relationships to surrounding structures, and maximum length, height (midline and lateral), and thickness (midline). Subsequently, the ligament was resected sharply in 1 piece that was several millimeters medial to its origin at the occipital condyle and superior margin of the C-1 lamina. It was then dissected off the dura and submitted for histological analysis.

After the specimens were received in 10% formalin in the laboratory, they were dissected and sectioned longitudinally and cross-sectioned at the edges. The specimens were then processed in the tissue processor and eventually placed into paraffin blocks. Tissue sections were cut from the paraffin blocks to 4-μm-thick sections and applied to glass slides. The slides were then stained with H & E and Masson's trichrome stain. Sections were evaluated for maximum thickness (in millimeters), hyaline nodules, calcifications, ossification, adipose tissue content, and fibrous splitting of the collagen fibers. They were examined using routine microscopy, and any areas of hyalinized nodularity were noted and measured at ×200 magnification (×20 objective with ×10 ocular lens) and essentially turned out to be 1 mm2. This is where a medium-power magnification field (MPF) of ×200 constituted essentially 1 mm2. The result of the histological evaluation of the suboccipital ligament for hyaline nodules, calcification, and ossification was graded as 2+ if present in 3 or more MPFs; 1+ if present in 1–2 MPFs; and 0, if present in less than 1 MPF. This grading scale was instituted to compare specimens objectively with previous histological evaluations.

We analyzed the various characteristics of the patients and compared these data according to numerous parameters, which were tested statistically (Tables 14).

TABLE 1.

Clinical characteristics and ligament dimensions by subgroup

CharacteristicCM-I PatientsNon–CM-I Patientsp Value*
Median (95% CI)Min–MaxMedian (95% CI)Min–Max
Age, yrs35 (29.6–43.4)19–7357 (52.1–61.3)48–71<0.001
Patient height, in66 (65.0–67.4)59–7566 (60.5–72.0)59–720.595
Weight, lbs169 (160.6–226.1)128–302175 (151.9–222.7)148–2400.778
BMI, kg/m228.3 (26.5–34.2)20.1–53.529.2 (21.9–40.0)20.1–48.70.534
Occipital ligament, mm
  Length34.3 (32.2–37.0)27–4135 (33.4–41.4)31–430.369
  Height at the midline10 (9.0–12.2)7–169 (8.5–12.5)8–130.733
  Height lateral10 (9.0–11.7)6–2011.5 (6.8–14.2)6–150.838
  Thickness at midline0.45 (0.3–0.5)0.2–10.4 (0.3–0.5)0.2–0.70.716
Cerebellar tonsil descent, mm8 (7–10)4–8.4NANANA

Max = maximum; min = minimum; NA = not applicable.

Determined using the Mann-Whitney U-test.

Statistically significant at p < 0.05.

TABLE 2.

Correlation of ligament measurements and sex

Occipital LigamentMaleFemaleTotalp Value*
Length1.3 (1–1.75)1.6 (1.18–2)1.5 (1.1–2)0.152
Height0.7 (0.6–0.95)0.6 (0.5–1)0.7 (0.5–1)0.838
Thickness0.5 (0.33–0.5)0.4 (0.3–0.55)0.4 (0.3–0.5)0.709

All values are shown in centimeters as the median (interquartile range) unless indicated otherwise.

Determined using the Mann-Whitney U-test.

TABLE 3.

Correlation of ligament measurements, BMI, and height

Occipital LigamentBMIHeight
Length0.300 (0.080)−0.207 (0.232)
Height0.207 (0.206)−0.173 (0.291)
Thickness0.139 (0.471)0.184 (0.339)

All values are shown as Spearman's rho correlation coefficient (p value).

TABLE 4.

Clinical characteristics of the patient subgroups

CharacteristicCM-I PatientsNon–CM-I PatientsTotalp Value*
Sex
  Male5 (16)4 (50)9 (23)0.065
  Female26 (84)4 (50)30 (77)
Syrinx
  Absent23 (74)8 (100)31 (80)0.168
  Present8 (26)08 (20)
Smoking status
  Nonsmoker18 (58)6 (75)24 (62)0.851
  Smoker8 (26)1 (12.5)9 (23)
  Former smoker5 (16)1 (12.5)6 (15)
Alcohol use
  No23 (74)7 (87)30 (77)>0.950
  Yes8 (26)1 (13)9 (23)
Diabetes
  No27 (87)7 (88)34 (87)>0.950
  Yes4 (13)1 (12)5 (13)
History of hypertension
  No20 (65)3 (38)23 (59)0.235
  Yes11 (35)5 (62)16 (41)
Hydrocephalus
  No30 (97)6 (75)36 (92)0.101
  Yes1 (3)2 (25)3 (8)
Headache
  No3 (10)1 (14)4 (10)>0.950
  Yes28 (90)6 (86)35 (90)
Total31 (100)8 (100)39 (100)

All values are shown as the number of patients (%) unless otherwise indicated.

Determined using Fisher's exact test.

Results

Clinical Parameters

This study included 10 cadaveric specimens and 39 patients: 31 (80%) were CM-I patients and 8 (20%) patients had a non–CM-I pathology of the posterior cranial fossa (non–CM-I patients). The second group consisted of 4 patients with posterior fossa metastasis (2 from lung cancer and 2 from breast cancer), 1 patient with a posterior fossa meningioma, 1 patient with a cerebellar hemangioblastoma, 1 patient with an ependymoma, and 1 patient with a cerebellar stroke undergoing decompression for occlusion of the posterior inferior cerebellar artery (Figs. 15).

FIG. 1.
FIG. 1.

Non–CM-I patient. Intraoperative photograph of the suboccipital ligament (arrows). Note the posterior cranial fossa and spinal dura (D), C-1 postlaminectomy edge (C1), and C-2 spinous process (C2). Figure is available in color online only.

FIG. 2.
FIG. 2.

CM-I patient. A: Intraoperative photograph of the suboccipital ligament (arrows). Before removing the occipital bone (B), the lower part of the ligament is not covered by bone (arrows) and spinal dura (D). B: The same patient after the bone has been removed. The suboccipital ligament is now completely uncovered (arrows). The suboccipital ligament superior or condylar (SB) and inferior atlantal branches (IB), posterior fossa and spinal dura (D), post–C-1 laminectomy edge (C1), and C-2 spinous process (C2) are shown. C: In the same patient, the right side of the ligament is shown at higher magnification. Figure is available in color online only.

FIG. 3.
FIG. 3.

Artistic rendering of the suboccipital ligament. A: Before removing the occipital bone. B: After the occipital bone is removed. C: Sagittal view of the same area on the right side. C0 = occiput; PAOM = posterior atlantooccipital membrane; RCPMi = rectus capitis posterior minor muscle. Copyright Ron Tribell. Published with permission.

FIG. 4.
FIG. 4.

Non–CM-I patient with a posterior fossa meningioma. A: Collagenous connective tissue of the suboccipital ligament and longitudinal section, including the adipose tissue. The fibers are roughly parallel. H & E stain, original magnification ×40 magnification. B: Medium-power magnification of the longitudinal section of the collagenous tissue also demonstrating the parallel nature of the fibers. H & E stain, original magnification ×200. C: A longitudinal section of the collagenous tissue. Masson's trichrome stain (original magnification ×200) highlights the parallel nature of the fibers. D: A cross-section of collagenous tissue–containing capillaries. H & E stain, original magnification ×400. Figure is available in color online only.

FIG. 5.
FIG. 5.

CM-I patient. A: Longitudinal section of the collagenous connective tissue of the suboccipital ligament. The collagen is interspersed with adipose tissue. Low-power magnification suggests some degree of change in the orientation of the collagenous fibrous tissue. H & E stain, original magnification ×40. B: Medium-power magnification of a longitudinal section of collagen tissue of the occipital ligament. The collagen exhibits some directional change in the fibers. H & E stain, original magnification ×200. C: Masson's trichrome stain (original magnification ×200) of the longitudinal section highlighting the directional change of the collagenous fibers. D: A cross-section of collagenous fibrous tissue. H & E stain, original magnification ×400. E: Hyaline nodule (asterisk). The arrows indicate the nodule interface. H & E stain, original magnification ×40). F: Hyaline nodule (asterisk). The arrows indicate the nodule interface. H & E stain, original magnification ×100. G: Masson's trichrome stain (original magnification ×40) highlights the same nodule (asterisk). Figure is available in color online only.

The median age of the patients was 43 years (range 19–73 years; interquartile range 29–54 years). CM-I patients were significantly younger than non–CM-I patients (median age 35 vs 57 years). There was no statistically significant difference in weight, height, and body mass index (BMI) between patient groups. There was also no statistically significant difference in the width or height of the ligaments between the CM-I and non–CM-I subgroups, either in the midline or laterally. The median descent of the cerebellar tonsils in CM-I patients was 8 mm, with a 95% CI of 7–10 mm (Table 1).

CM-I patients were more commonly women, whereas the sexes were equally distributed among non–CM-I patients. A syrinx was noted in 8 CM-I patients (20%). Among all patients, 9 (23%) patients were smokers, 9 (23%) patients consumed alcohol on a weekly basis, and 5 (13%) patients had diabetes mellitus. Sixteen (41%) patients had a history of hypertension, 3 (8%) patients had hydrocephalus, and 35 (90%) patients had a history of severe headaches. There were no significant differences between the patient subgroups in any of the parameters (Table 4).

There were also no significant differences in the dimensions of the ligament between the sexes (Table 2), nor was there any significant correlation between the BMI or height of patients and the dimensions of the ligament (Table 3). There was neither a statistically significant correlation between the suboccipital ligament dimensions (length, height, thickness) and BMI, nor between the suboccipital ligament measurements and the height of patients (Table 3). There were no statistically significant differences between the CM-I and non–CM-I patient subgroups regarding smoking history, alcohol consumption, and presence of diabetes mellitus, hypertension, hydrocephalus, and headaches (Table 4).

Anatomy

The suboccipital ligament and the posterior suboccipital membrane are 2 completely separate structures and should not be mutually confused. The ligament is located ventral and the membrane is dorsal to the occipital bone. More precisely, the posterior suboccipital membrane is located between the occipital bone and C-1 lamina, which are anterior (ventral) to it, and the rectus capitis posterior major and minor, which are posterior (dorsal) to it. The posterior suboccipital membrane extends between the dorsal surfaces of the occipital bone and C-1 lamina with its fibers oriented vertically. In all of our cadaveric specimens, as well as intraoperatively, we dissected and removed the posterior suboccipital membrane before studying the suboccipital ligament.

The suboccipital ligament is located ventral (anterior) to the occipital bone (Figs. 13). Approximately two-thirds of the ligament height is covered by the occipital bone, while one-third extends below the occipital rim and ends at the upper portion of the atlantooccipital interspace (Fig. 2A). It extends horizontally between the bilateral occipital condyles and superior rims of the C-1 laminae with separate branches: the condyle (superior) branch and the C-1 or atlantal (inferior) branch. These 2 branches immediately unite to form a ligament with horizontally oriented fibers. Its general shape is a curved rectangle. It has a median length of 35 mm, a height of 10 mm, and a thickness of 0.5 mm (Figs. 1,2B and C, and 3).

In its middle third, the ligament is loosely attached to the dura, which is located anteriorly and can be easily dissected from it during surgery. Laterally, toward the lateral third, it becomes more densely attached to the dura, making mutual separation slightly more difficult. The suboccipital ligament is a clearly distinct structure from the dura and can be dissected from it. Therefore, calling it a dural band does not emphasize that these are 2 different structures.

Histology

The ligament tissue in the CM-I patients was generally more disorganized than that in the non–CM-I subgroup, with poorly arranged collagen bands and interspersed adipose tissue (Figs. 4A–D and 5A–G). Furthermore, as a group, the CM-I patients had more hyalinized fibrosis than the non–CM-I subgroup. These patients also showed changes in the direction of the fibers. The CM-I group had hyaline nodules that ranged from Grade 0 to 2+. The nodules in 5 patients were graded as 2+, the nodules in 17 patients were graded as 1+, and the nodules in 9 patients were graded as 0. Of the 8 patients in the non–CM-I group, all were graded as 0 for hyaline nodules. Masson's trichrome stain was quite helpful in accentuating the hyaline nodules (Fig. 5F and G). There were differences in the degree of hyalinization of the hyaline nodules.

Two of the patients in the CM-I group were found to have Grade 1+ calcifications, whereas none of the patients in the non–CM-I group showed identifiable calcifications. No definitive ossification was seen in the surgical pathology specimens of either group. The non–CM-I group had a uniformly horizontal orientation of the fibers without any significant alteration.

Collagen fiber splitting was identified, and a blinded study was carried out on the tissue sections in which there was no identifiable difference between the amount of collagen fiber splitting in the CM-I and non–CM-I patients. Adipose tissue was seen in all patients, some having very little while others had more, but there was no detectable difference between groups regarding adipose tissue.

Discussion

Many neurosurgeons are aware of the existence of the suboccipital ligament as an important anatomical structure and landmark at the craniocervical junction and posterior cranial fossa that they encounter daily in surgery. On the other hand, other neurosurgeons see that ligament as part of the dura, or the posterior atlantooccipital membrane, or as an unusually thickened fibrous band without knowing precisely the location and anatomy of this structure. In addition, this ligament is perceived to be “hypertrophic” in patients with CM-I and contributes significantly to CM-I pathology.1–3,5–19,21–42 To the best of our knowledge, this is the first and only study that has investigated—in real time and prospectively—the cadaveric, intraoperative, and histological aspects of this anatomical structure.

Anatomy, Location, Function, and Name

The suboccipital ligament is located precisely at the junction of the spinal and posterior cranial fossa dura. It serves as an outside boundary separating the 2 dural compartments and creates a fibrous suspension or constriction between the bulky, bilobar dura and covers the 2 cerebellar hemispheres superiorly (rostrally) and the cylindrically shaped spinal dura inferiorly (caudally). One may speculate that this ligament serves physiologically as a “suspension” of the cranial dural compartment.

The ligament also adheres partially to the occipital bone dorsally. On the basis of its course and origins, we hypothesized that the suboccipital ligament—by connecting the bilateral condylar joints, the lateral parts of the C-1 laminae, and the occipital bone—helps increase the rotational stability of the craniocervical junction. Due to its suboccipital location at the lower edge of the occipital bone (i.e., the foramen magnum posterior rim), we propose that the best name for this structure is the “suboccipital ligament.”

General Surgical Implications

One of the reasons investigators have neglected to study this ligament may be because of local bleeding from the epidural venous plexus and suboccipital cavernous sinus during surgery in the area.4 This problem was eliminated with the usage of Gelfoam hemostatic powder. The other reason for neglecting the ligament may be the fact that some surgeons may have considered it to be part of the thickened dura or inadvertently removed parts of it during the suboccipital craniectomy.

We cannot overemphasize the importance of ligament dissection and controlled resection to separate it from the dura. Once the ligament is removed, we can proceed with a Y-shaped incision, or any other dural incision, making it easier to preserve the arachnoid membrane, as some authors choose to avoid opening the dura during CM-I decompression.40 Several authors report an immediate enlargement of craniocervical junction stenosis in CM-I patients, even before or without dural opening and after incision of the ligament.11,22–24,29,40,42 Our recent review of CM-I series from 1965 to 2013 showed that in 3% of adult, 19% of pediatric, and 5% of combined CM-I series, surgeons did not open the dura after suboccipital bone decompression and incision of the ligament. This attitude clearly reflects the importance of this ligament and its complete resection in CM-I decompression. Furthermore, by removing the ligament and thus preserving an even thickness of dural edges above, below, and at the level of the ligament, subsequent suturing of the dural graft to the dura becomes easier and more successfully prevents a CSF leak or pseu-domeningocele formation.

Histology

Several histological studies of cadaveric specimens have been done in the proximity of the suboccipital ligament but have failed to investigate it per se. Chauvet et al. histologically studied the dura of the posterior cranial fossa in cadavers,12 but it is unclear whether they removed all of the superficial layers, including the suboccipital ligament, or included them in the study. Dean and Mitchell studied the macroscopic relationships between the nuchal ligament and the spinal dura without removing the occipital bone.13 Scali et al. studied the rectus capitis posterior major myodural bridge to the cervical dura.31 Nash et al. carried out a sheet plastination and microscopic study on the configuration of the connective tissue in the posterior atlantooccipital interspace with axial and sagittal sections.26 Understandably, their study could not provide a 3D evaluation of the anatomical area and the suboccipital ligament specifically.

In their histological study, Nakamura et al. studied what they called “the outer dural layer/dural band” pathology in patients with CM-I and syringomyelia and compared it with cadaveric specimens.25 Their study included the whole “dural band–posterior cranial fossa dura complex,” which we suspect included the dura and suboccipital ligament en bloc. Half of their 8 CM-I specimens included calcifications, and 6 of the 8 specimens showed ossifications.25 However, as there is significant bone drilling during the approach, we must interpret those findings of the presence of “calcifications” cautiously. Fiber splitting, fiber branching, and hyaline nodules were found in all of their CM-I surgical specimens. The rounded, nodular structures seen in the CM-I surgical specimens were named “hyaline nodules.”25

We also found that the ligament tissue in the CM-I patients was generally more disorganized, with poorly arranged collagen bands and interspersed adipose tissue, than in comparison with the non–CM-I subgroup. There was also more hyalinized fibrosis than in the non–CM-I subgroup, including some degree of change in the orientation of the collagenous fibrous tissue. The other real and significant difference was the frequent presence of hyaline nodules in the suboccipital ligaments of the CM-I patients and the complete absence of them in the non–CM-I subgroup. The explanation for this difference requires further study. Overall, these histological differences may be an additional reflection of the alterations in mesodermal development that exist in the area of the posterior cranial fossa in CM-I patients.

Comparison of Groups

The only significant clinical differences between the CM-I and non–CM-I groups were the female predominance in the CM-I group and the ages of the patients. The CM-I group had a younger mean age. There was no difference between the subgroups regarding all other clinical parameters. However, the association of increased BMI and CM-I has been previously reported.4

The results of our study clearly dispute the myth that the suboccipital ligament is “hypertrophied” in CM-I patients as opposed to patients with other pathologies. We can hypothesize that this false intraoperative impression of a hypertrophied ligament is based on the fact that CM-I patients have a significantly smaller volume of the posterior cranial fossa, as proven by many volumetric studies of CM-I patients.7,8,34,38 Therefore, the ligament looks larger compared with the smaller size of the posterior cranial fossa in CM-I patients, when in fact it is the same size in all patients.

Conclusions

We described in detail the horizontally oriented fibrous structure at the dorsal craniocervical junction area, which we named the “suboccipital ligament.” It has horizontally oriented hyaline fibers and a median length of 35 mm, height of 10 mm, and thickness of 0.5 mm. It extends between the occipital condyle and the superior edge of the C-1 lamina, connecting contralateral sides and appearing to function as a real ligament. It is located ventral to the occipital bone, which covers approximately two-thirds of the height of the ligament. It is loosely attached to the dura medially, and the attachment becomes firmer laterally. The ligament can therefore be easily detached from the dura and resected in the median part, thus enabling a sharp dural incision with clear edges. This enables precise dural suturing during closure.

The dimensions of the ligament are not significantly different between CM-I and non–CM-I patients; therefore, in CM-I patients, the ligament is not hypertrophied.

The ligamentous histology shows structural differences between CM-I and non–CM-I patients, most notably the presence of hyaline nodules and an altered fiber orientation in CM-I patients. This may be a reflection of the differences that exist in the mesodermal development of the posterior cranial fossa in CM-I patients.

Acknowledgments

We would like to thank Mr. Ron Tribell for his artwork, Ms. Kristina Kralik for statistical expertise, Ms. Julie Yamamoto for editing the manuscript, and Mr. Andrew J. Gienapp for copyediting, preparation of the manuscript and figures, and publication assistance.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Arnautovic, Bugg, Splavski. Acquisition of data: Arnautovic, Alabaster. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Arnautovic. Statistical analysis: all authors. Study supervision: Arnautovic, Bugg, Splavski.

References

  • 1

    Alden TD, Ojemann JG, Park TS: Surgical treatment of Chiari I malformation: indications and approaches. Neurosurg Focus 11:1 E2, 2001

  • 2

    Anderson RC, Emerson RG, Dowling KC, Feldstein NA: Improvement in brainstem auditory evoked potentials after suboccipital decompression in patients with Chiari I malformations. J Neurosurg 98:459464, 2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Arnautovic A, Splavski B, Boop FA, Arnautovic KI: Pediatric and adult Chiari malformation Type I surgical series 1965–2013: a review of demographics, operative treatment, and outcomes. J Neurosurg Pediatr 15:161177, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Arnautović KI, al-Mefty O, Pait TG, Krisht AF, Husain MM: The suboccipital cavernous sinus. J Neurosurg 86:252262, 1997

  • 5

    Arnautovic KI, Muzevic D, Splavski B, Boop FA: Association of increased body mass index with Chiari malformation Type I and syrinx formation in adults. J Neurosurg 119:10581067, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Arora P, Behari S, Banerji D, Chhabra DK, Jain VK: Factors influencing the outcome in symptomatic Chiari I malformation. Neurol India 52:470474, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Aydin S, Hanimoglu H, Tanriverdi T, Yentur E, Kaynar MY: Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surg Neurol 64:237241, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Badie B, Mendoza D, Batzdorf U: Posterior fossa volume and response to suboccipital decompression in patients with Chiari I malformation. Neurosurgery 37:214218, 1995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Banerji NK, Millar JH: Chiari malformation presenting in adult life. Its relationship to syringomyelia. Brain 97:157168, 1974

  • 10

    Bell WO, Charney EB, Bruce DA, Sutton LN, Schut L: Symptomatic Arnold-Chiari malformation: review of experience with 22 cases. J Neurosurg 66:812816, 1987

  • 11

    Caldarelli M, Novegno F, Vassimi L, Romani R, Tamburrini G, Di Rocco C: The role of limited posterior fossa craniectomy in the surgical treatment of Chiari malformation Type I: experience with a pediatric series. J Neurosurg 106:3 Suppl 187195, 2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Chauvet D, Carpentier A, George B: Dura splitting decompression in Chiari type 1 malformation: clinical experience and radiological findings. Neurosurg Rev 32:465470, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Dean NA, Mitchell BS: Anatomic relation between the nuchal ligament (ligamentum nuchae) and the spinal dura mater in the craniocervical region. Clin Anat 15:182185, 2002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Di X: Endoscopic suboccipital decompression on pediatric Chiari type I. Minim Invasive Neurosurg 52:119125, 2009

  • 15

    Eicker SO, Mende KC, Dührsen L, Schmidt NO: Minimally invasive approach for small ventrally located intradural lesions of the craniovertebral junction. Neurosurg Focus 38:4 E10, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Eisenstat DD, Bernstein M, Fleming JF, Vanderlinden RG, Schutz H: Chiari malformation in adults: a review of 40 cases. Can J Neurol Sci 13:221228, 1986

  • 17

    Erdogan E, Cansever T, Secer HI, Temiz C, Sirin S, Kabatas S, : The evaluation of surgical treatment options in the Chiari malformation type I. Turk Neurosurg 20:303313, 2010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Godil SS, Parker SL, Zuckerman SL, Mendenhall SK, McGirt MJ: Accurately measuring outcomes after surgery for adult Chiari I malformation: determining the most valid and responsive instruments. Neurosurgery 72:820827, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Goel A, Bhatjiwale M, Desai K: Basilar invagination: a study based on 190 surgically treated patients. J Neurosurg 88:962968, 1998

  • 20

    Gray H, Warwick R, Williams PL: Gray's Anatomy ed 36 Philadelphia, Saunders, 1980

  • 21

    Klekamp J: Surgical treatment of Chiari I malformation—analysis of intraoperative findings, complications, and outcome for 371 foramen magnum decompressions. Neurosurgery 71:365380, 2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Kotil K, Ton T, Tari R, Savas Y: Delamination technique together with longitudinal incisions for treatment of Chiari I/syringomyelia complex: a prospective clinical study. Cerebrospinal Fluid Res 6:7, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Litvack ZN, Lindsay RA, Selden NR: Dura splitting decompression for Chiari I malformation in pediatric patients: clinical outcomes, healthcare costs, and resource utilization. Neurosurgery 72:922929, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Massimi L, Caldarelli M, Paternoster G, Novegno F, Tamburrini G, Di Rocco C: Miniinvasive surgery for Chiari type I malformation. Neuroradiol J 21:6570, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Nakamura N, Iwasaki Y, Hida K, Abe H, Fujioka Y, Nagashima K: Dural band pathology in syringomyelia with Chiari type I malformation. Neuropathology 20:3843, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Nash L, Nicholson H, Lee AS, Johnson GM, Zhang M: Configuration of the connective tissue in the posterior atlanto-occipital interspace: a sheet plastination and confocal microscopy study. Spine (Phila Pa 1976) 30:13591366, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Park JK, Gleason PL, Madsen JR, Goumnerova LC, Scott RM: Presentation and management of Chiari I malformation in children. Pediatr Neurosurg 26:190196, 1997

  • 28

    Paul KS, Lye RH, Strang FA, Dutton J: Arnold-Chiari malformation. Review of 71 cases. J Neurosurg 58:183187, 1983

  • 29

    Romero FR, Pereira CA: Suboccipital craniectomy with or without duraplasty: what is the best choice in patients with Chiari type 1 malformation?. Arq Neuropsiquiatr 68:623626, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sala F, Squintani G, Tramontano V, Coppola A, Gerosa M: Intraoperative neurophysiological monitoring during surgery for Chiari malformations. Neurol Sci 32:Suppl 3 S317S319, 2011

    • Search Google Scholar
    • Export Citation
  • 31

    Scali F, Pontell ME, Enix DE, Marshall E: Histological analysis of the rectus capitis posterior major's myodural bridge. Spine J 13:558563, 2013

  • 32

    Schut L, Bruce DA: The Arnold-Chiari malformation. Orthop Clin North Am 9:913921, 1978

  • 33

    Smith J, Ridley A: Cerebellar ectopia presenting in adult life. BMJ 1:353355, 1969

  • 34

    Stovner LJ, Bergan U, Nilsen G, Sjaastad O: Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:113118, 1993

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Takayasu M, Takagi T, Hara M, Anzai M: A simple technique for expansive suboccipital cranioplasty following foramen magnum decompression for the treatment of syringomyelia associated with Chiari I malformation. Neurosurg Rev 27:173177, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Tubbs RS, Beckman J, Naftel RP, Chern JJ, Wellons JC III, Rozzelle CJ, : Institutional experience with 500 cases of surgically treated pediatric Chiari malformation Type I. J Neurosurg Pediatr 7:248256, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Tubbs RS, Wellons JC III, Oakes WJ, Blount JP: Reformation of the posterior atlanto-occipital membrane following posterior fossa decompression with subsequent constriction at the craniocervical junction. Pediatr Neurosurg 38:219221, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Vanaclocha V, Saiz-Sapena N, Garcia-Casasola MC: Surgical technique for craniocervical decompression in syringomyelia associated with Chiari type I malformation. Acta Neurochir (Wien) 139:529540, 1997

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Vega A, Quintana F, Berciano J: Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99:137145, 1990

  • 40

    Yundt KD, Park TS, Tantuwaya VS, Kaufman BA: Posterior fossa decompression without duraplasty in infants and young children for treatment of Chiari malformation and achondroplasia. Pediatr Neurosurg 25:221226, 1996

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Zamel K, Galloway G, Kosnik EJ, Raslan M, Adeli A: Intraoperative neurophysiologic monitoring in 80 patients with Chiari I malformation: role of duraplasty. J Clin Neurophysiol 26:7075, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Zhou DB, Zhao JZ, Zhang D, Zhao YL: Suboccipital bony decompression combined with removal of the dural band as treatment for Chiari I malformation. Chin Med J (Engl) 117:12741277, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Contributor Notes

Correspondence Kenan I. Arnautovic, Semmes-Murphey Clinic, 6325 Humphreys Blvd., Memphis, TN 38120. email: kenanarnaut@yahoo.com.

INCLUDE WHEN CITING Published online April 14, 2017; DOI: 10.3171/2016.10.JNS162161.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • View in gallery

    Non–CM-I patient. Intraoperative photograph of the suboccipital ligament (arrows). Note the posterior cranial fossa and spinal dura (D), C-1 postlaminectomy edge (C1), and C-2 spinous process (C2). Figure is available in color online only.

  • View in gallery

    CM-I patient. A: Intraoperative photograph of the suboccipital ligament (arrows). Before removing the occipital bone (B), the lower part of the ligament is not covered by bone (arrows) and spinal dura (D). B: The same patient after the bone has been removed. The suboccipital ligament is now completely uncovered (arrows). The suboccipital ligament superior or condylar (SB) and inferior atlantal branches (IB), posterior fossa and spinal dura (D), post–C-1 laminectomy edge (C1), and C-2 spinous process (C2) are shown. C: In the same patient, the right side of the ligament is shown at higher magnification. Figure is available in color online only.

  • View in gallery

    Artistic rendering of the suboccipital ligament. A: Before removing the occipital bone. B: After the occipital bone is removed. C: Sagittal view of the same area on the right side. C0 = occiput; PAOM = posterior atlantooccipital membrane; RCPMi = rectus capitis posterior minor muscle. Copyright Ron Tribell. Published with permission.

  • View in gallery

    Non–CM-I patient with a posterior fossa meningioma. A: Collagenous connective tissue of the suboccipital ligament and longitudinal section, including the adipose tissue. The fibers are roughly parallel. H & E stain, original magnification ×40 magnification. B: Medium-power magnification of the longitudinal section of the collagenous tissue also demonstrating the parallel nature of the fibers. H & E stain, original magnification ×200. C: A longitudinal section of the collagenous tissue. Masson's trichrome stain (original magnification ×200) highlights the parallel nature of the fibers. D: A cross-section of collagenous tissue–containing capillaries. H & E stain, original magnification ×400. Figure is available in color online only.

  • View in gallery

    CM-I patient. A: Longitudinal section of the collagenous connective tissue of the suboccipital ligament. The collagen is interspersed with adipose tissue. Low-power magnification suggests some degree of change in the orientation of the collagenous fibrous tissue. H & E stain, original magnification ×40. B: Medium-power magnification of a longitudinal section of collagen tissue of the occipital ligament. The collagen exhibits some directional change in the fibers. H & E stain, original magnification ×200. C: Masson's trichrome stain (original magnification ×200) of the longitudinal section highlighting the directional change of the collagenous fibers. D: A cross-section of collagenous fibrous tissue. H & E stain, original magnification ×400. E: Hyaline nodule (asterisk). The arrows indicate the nodule interface. H & E stain, original magnification ×40). F: Hyaline nodule (asterisk). The arrows indicate the nodule interface. H & E stain, original magnification ×100. G: Masson's trichrome stain (original magnification ×40) highlights the same nodule (asterisk). Figure is available in color online only.

  • 1

    Alden TD, Ojemann JG, Park TS: Surgical treatment of Chiari I malformation: indications and approaches. Neurosurg Focus 11:1 E2, 2001

  • 2

    Anderson RC, Emerson RG, Dowling KC, Feldstein NA: Improvement in brainstem auditory evoked potentials after suboccipital decompression in patients with Chiari I malformations. J Neurosurg 98:459464, 2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Arnautovic A, Splavski B, Boop FA, Arnautovic KI: Pediatric and adult Chiari malformation Type I surgical series 1965–2013: a review of demographics, operative treatment, and outcomes. J Neurosurg Pediatr 15:161177, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Arnautović KI, al-Mefty O, Pait TG, Krisht AF, Husain MM: The suboccipital cavernous sinus. J Neurosurg 86:252262, 1997

  • 5

    Arnautovic KI, Muzevic D, Splavski B, Boop FA: Association of increased body mass index with Chiari malformation Type I and syrinx formation in adults. J Neurosurg 119:10581067, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Arora P, Behari S, Banerji D, Chhabra DK, Jain VK: Factors influencing the outcome in symptomatic Chiari I malformation. Neurol India 52:470474, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Aydin S, Hanimoglu H, Tanriverdi T, Yentur E, Kaynar MY: Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surg Neurol 64:237241, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Badie B, Mendoza D, Batzdorf U: Posterior fossa volume and response to suboccipital decompression in patients with Chiari I malformation. Neurosurgery 37:214218, 1995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Banerji NK, Millar JH: Chiari malformation presenting in adult life. Its relationship to syringomyelia. Brain 97:157168, 1974

  • 10

    Bell WO, Charney EB, Bruce DA, Sutton LN, Schut L: Symptomatic Arnold-Chiari malformation: review of experience with 22 cases. J Neurosurg 66:812816, 1987

  • 11

    Caldarelli M, Novegno F, Vassimi L, Romani R, Tamburrini G, Di Rocco C: The role of limited posterior fossa craniectomy in the surgical treatment of Chiari malformation Type I: experience with a pediatric series. J Neurosurg 106:3 Suppl 187195, 2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Chauvet D, Carpentier A, George B: Dura splitting decompression in Chiari type 1 malformation: clinical experience and radiological findings. Neurosurg Rev 32:465470, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Dean NA, Mitchell BS: Anatomic relation between the nuchal ligament (ligamentum nuchae) and the spinal dura mater in the craniocervical region. Clin Anat 15:182185, 2002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Di X: Endoscopic suboccipital decompression on pediatric Chiari type I. Minim Invasive Neurosurg 52:119125, 2009

  • 15

    Eicker SO, Mende KC, Dührsen L, Schmidt NO: Minimally invasive approach for small ventrally located intradural lesions of the craniovertebral junction. Neurosurg Focus 38:4 E10, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Eisenstat DD, Bernstein M, Fleming JF, Vanderlinden RG, Schutz H: Chiari malformation in adults: a review of 40 cases. Can J Neurol Sci 13:221228, 1986

  • 17

    Erdogan E, Cansever T, Secer HI, Temiz C, Sirin S, Kabatas S, : The evaluation of surgical treatment options in the Chiari malformation type I. Turk Neurosurg 20:303313, 2010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Godil SS, Parker SL, Zuckerman SL, Mendenhall SK, McGirt MJ: Accurately measuring outcomes after surgery for adult Chiari I malformation: determining the most valid and responsive instruments. Neurosurgery 72:820827, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Goel A, Bhatjiwale M, Desai K: Basilar invagination: a study based on 190 surgically treated patients. J Neurosurg 88:962968, 1998

  • 20

    Gray H, Warwick R, Williams PL: Gray's Anatomy ed 36 Philadelphia, Saunders, 1980

  • 21

    Klekamp J: Surgical treatment of Chiari I malformation—analysis of intraoperative findings, complications, and outcome for 371 foramen magnum decompressions. Neurosurgery 71:365380, 2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Kotil K, Ton T, Tari R, Savas Y: Delamination technique together with longitudinal incisions for treatment of Chiari I/syringomyelia complex: a prospective clinical study. Cerebrospinal Fluid Res 6:7, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Litvack ZN, Lindsay RA, Selden NR: Dura splitting decompression for Chiari I malformation in pediatric patients: clinical outcomes, healthcare costs, and resource utilization. Neurosurgery 72:922929, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Massimi L, Caldarelli M, Paternoster G, Novegno F, Tamburrini G, Di Rocco C: Miniinvasive surgery for Chiari type I malformation. Neuroradiol J 21:6570, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Nakamura N, Iwasaki Y, Hida K, Abe H, Fujioka Y, Nagashima K: Dural band pathology in syringomyelia with Chiari type I malformation. Neuropathology 20:3843, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Nash L, Nicholson H, Lee AS, Johnson GM, Zhang M: Configuration of the connective tissue in the posterior atlanto-occipital interspace: a sheet plastination and confocal microscopy study. Spine (Phila Pa 1976) 30:13591366, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Park JK, Gleason PL, Madsen JR, Goumnerova LC, Scott RM: Presentation and management of Chiari I malformation in children. Pediatr Neurosurg 26:190196, 1997

  • 28

    Paul KS, Lye RH, Strang FA, Dutton J: Arnold-Chiari malformation. Review of 71 cases. J Neurosurg 58:183187, 1983

  • 29

    Romero FR, Pereira CA: Suboccipital craniectomy with or without duraplasty: what is the best choice in patients with Chiari type 1 malformation?. Arq Neuropsiquiatr 68:623626, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sala F, Squintani G, Tramontano V, Coppola A, Gerosa M: Intraoperative neurophysiological monitoring during surgery for Chiari malformations. Neurol Sci 32:Suppl 3 S317S319, 2011

    • Search Google Scholar
    • Export Citation
  • 31

    Scali F, Pontell ME, Enix DE, Marshall E: Histological analysis of the rectus capitis posterior major's myodural bridge. Spine J 13:558563, 2013

  • 32

    Schut L, Bruce DA: The Arnold-Chiari malformation. Orthop Clin North Am 9:913921, 1978

  • 33

    Smith J, Ridley A: Cerebellar ectopia presenting in adult life. BMJ 1:353355, 1969

  • 34

    Stovner LJ, Bergan U, Nilsen G, Sjaastad O: Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:113118, 1993

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Takayasu M, Takagi T, Hara M, Anzai M: A simple technique for expansive suboccipital cranioplasty following foramen magnum decompression for the treatment of syringomyelia associated with Chiari I malformation. Neurosurg Rev 27:173177, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Tubbs RS, Beckman J, Naftel RP, Chern JJ, Wellons JC III, Rozzelle CJ, : Institutional experience with 500 cases of surgically treated pediatric Chiari malformation Type I. J Neurosurg Pediatr 7:248256, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Tubbs RS, Wellons JC III, Oakes WJ, Blount JP: Reformation of the posterior atlanto-occipital membrane following posterior fossa decompression with subsequent constriction at the craniocervical junction. Pediatr Neurosurg 38:219221, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Vanaclocha V, Saiz-Sapena N, Garcia-Casasola MC: Surgical technique for craniocervical decompression in syringomyelia associated with Chiari type I malformation. Acta Neurochir (Wien) 139:529540, 1997

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Vega A, Quintana F, Berciano J: Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99:137145, 1990

  • 40

    Yundt KD, Park TS, Tantuwaya VS, Kaufman BA: Posterior fossa decompression without duraplasty in infants and young children for treatment of Chiari malformation and achondroplasia. Pediatr Neurosurg 25:221226, 1996

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Zamel K, Galloway G, Kosnik EJ, Raslan M, Adeli A: Intraoperative neurophysiologic monitoring in 80 patients with Chiari I malformation: role of duraplasty. J Clin Neurophysiol 26:7075, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Zhou DB, Zhao JZ, Zhang D, Zhao YL: Suboccipital bony decompression combined with removal of the dural band as treatment for Chiari I malformation. Chin Med J (Engl) 117:12741277, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 746 0 0
Full Text Views 601 306 38
PDF Downloads 247 93 9
EPUB Downloads 0 0 0