Defining limits of foramen magnum decompression in Chiari I malformation to prevent complications related to cerebellar migration: An anatomico-radiological study

Abstract

Background:

Foramen magnum decompression (FMD) is the primary modality of treatment for symptomatic Chiari I malformation. However, the surgery is associated with cerebrospinal fluid (CSF) dynamic complications which may include non-improvement of symptoms, progression of syrinx, or cerebellar slump which are related to the size of decompression.

Objective:

The objective of the study was to define the limits of FMD to prevent CSF dynamic complications, including cerebellar ptosis.

Materials and Methods:

Anatomical relations of cerebellar tonsils and occipital bone were studied in 42 sagittal cut sections and 105 sagittal magnetic resonance imaging (MRI) sections. The limits of decompression were defined by our proposition of decompressing till the inferior semilunar fissure. In total, 27 patients underwent FMD and 21 were followed up.

Results:

Occipital bone in cut sections and MRI sections showed four configurations termed as single cusp, bicuspid, straight, and question-mark. Of these, straight and question-mark configurations were more commonly seen. Of the 21 patients who were followed up after FMD, all had good improvement with none developing features of CSF dynamic complications.

Conclusion:

The FMD surgery for Chiari I malformation should be performed with limits tailored to individual patients. Decompression should stop at the inferior semilunar fissure so as to prevent CSF dynamic complications, including cerebellar ptosis.

INTRODUCTION

Ever since its description by Hans Chiari, the Chiari I malformation has been a subject of varied opinions regarding optimal treatment methodology.[1] While the condition manifests itself in a small posterior fossa, herniating cerebellar tonsils, compromise of cerebrospinal fluid (CSF) dynamics, syrinx, and consequential neurological deficits, the treatment primarily comprises a revamp of posterior fossa and CV junction anatomy. This may include, in its various combinations, posterior fossa decompression, foramen magnum decompression (FMD), durotomy, duroplasty, dural band release, and “manipulation” of herniated tonsils. Recently, Goel has advocated atlanto-axial stabilization as a means of treating Chiari I malformation, hypothesizing that Chiari malformation is “nature’s airbag” to prevent injuries to neural elements resulting from atlanto-axial instability.[2] However, till such time as the hypothesis gains widespread acceptance, decompressive procedures shall remain in vogue.[3]

These procedures, however, carry with them the risk of no improvement in clinical features or even neurological worsening secondary to several factors compromising postoperative CSF dynamics, including cerebellar ptosis or slump, should the decompression cross a certain critical limit as first described by Williams.[4,5,6,7] This drag of the cerebellum on the dura and brainstem may lead to a number of complications, including persistence of syrinx and neurological deficits. In view of the above, a number of authors have attempted to define a set of criteria to set limits of decompression that achieve adequate decompression without causing cerebellar slump.

At our institution, we faced the complications of cerebellar ptosis in 2 consecutive patients. This led us to undertake the present clinico-anatomical study to identify radiological and anatomical landmarks which may define the limits of decompression, such that they may release the obstruction to CSF dynamics but prevent a cerebellar ptosis.

MATERIALS AND METHODS

Preoperative and postoperative imaging of patients who underwent FMD prior to January 2016 and had postoperative features of cerebellar ptosis or nonresolution of syrinx were studied in detail to delineate the extent of decompression. This was followed by a study of 42 sagittal cut sections of human skull and brain in mounted specimens and photographs, and a study of 105 sagittal magnetic resonance images (MRIs) of individuals without Chiari malformation to further our understanding of local bony anatomy and the relation of cerebellar tonsils to the same.

Between January 2016 and April 2018, a total of 27 patients with Chiari I malformation were treated by performing FMD. Such cases of Chiari I malformation during this period which had co-existent gross structural brain or spinal anomalies, hydrocephalus, tumor, infection, or connective tissue disorder, were not included in the study group.

Prior to the procedure, imaging of each of these patients was studied in detail, and anatomical landmarks congruent to those on cut sections were identified, and appropriate measurements were made to guide the extent of decompression intraoperatively. It was our proposition that the extent of decompression should not be measured in absolute numbers; the decompression should, on the other hand, not compromise cerebellar support while freeing up the tonsils at the same time. Our belief was that the inferior semilunar fissure, which demarcates the tonsils from the rest of the cerebellum, should form the boundary of decompression. Doing so would allow the tonsils enough space to remain free but would not compromise the cerebellar support.

These patients were followed up postoperatively, and imaging was repeated at 1 month, 3 months, 6 months, and 1-year intervals, with a minimum of 6 months follow-up.

Operative technique

Proposition

It was our proposition that the cerebellar ptosis occurs only in patients in whom the decompression crosses that boundary set by the inferior semilunar fissure. This removes the support for the main bulk of the cerebellar hemisphere, which may then slump downwards. In fact, we maintain that the cerebellar ptosis forms the end of a continuous spectrum of conditions resulting from an overzealous decompression which includes in its range conditions like a non-improvement of symptoms and nonresolution of syrinx. We believe that this occurs due to varying degrees of drag of cerebellar mass on the brain stem, leading to varying degrees of obstruction to CSF flow as well as direct traction-related insult to the brain stem. Following our study of cerebellar anatomy, we believed that the cerebellar tonsils behave as pedunculated structures and that freeing the tonsils would, in effect, provide enough freedom of CSF flow, and that cerebellar support need not be compromised, as it would add no further value to decompression.

The technique

All patients prior to surgery underwent a careful measurement of the distance from the lip of the foramen magnum to the inferior semilunar fissure, and the decompression was confined to the limits so determined.

This was followed by the removal of the posterior arch of the atlas to expose the cranio-vertebral junction (CVJ) dura. Crescent durotomy was performed in these cases as described by Panigrahi et al.[8] Tonsils were inspected, and should the CSF pulsations be seen, no further dissection was done. In cases where pulsations were not seen, arachnoid dissection with manipulation of tonsils was performed till the foramen of Magendie was visualized and tonsils were freed.

In case there was an inadvertent breach of the limits of decompression, it was made sure that the dural incision stays true to the limits that would have been dictated by the planned decompression, and thus cerebellar support is not compromised. Dura in such cases may be coagulated and thus “firmed up” to further maintain the integrity of cerebellar support.

Institution ethical committee approval and patient consent

The study was duly approved by the institutional ethical committee. Each of the patients was informed about the planned treatment and the options to the same, and informed consent was obtained from them.

RESULTS

Cut sections

In total, 42 cut sections of human skull and brain were reviewed. We found that the inner surface of the occipital bone from the superior nuchal line towards the foramen magnum had differing configurations in different anatomical specimens. Of the 42 sections studied, the bone showed a single cusp-like configuration in 8 specimens. In these specimens, the cusp held in it the cerebellar hemispheres while the tonsils protruded caudally. In the majority of the specimens, the occipital bone showed a “question-mark” like configuration wherein it had a cusp supporting the cerebellar hemispheres, followed by its ending in a straight line that bordered tonsils posteriorly. This configuration was seen in 20 specimens. Another variant that was noted in 12 specimens was a straight configuration that had no cusp. Two specimens showed a bicuspid configuration wherein the cerebellar hemispheres were contained in the superior cusp, and tonsils were bordered posteriorly by the inferior cusp [Figure 1 and Table 1].

Figure 1.

Diagrammatic, cut section, and magnetic resonance (MR) representation of the relation of tonsils (shaded darkly), cerebellum, and occipital bone configuration. In each row left panel shows a diagrammatic representation, the middle panel shows cut section anatomy, and the right panel shows MR imaging with red star marking the inferior semilunar fissure. (a-c) Depict question-mark configuration, (d-f) depict single cusp configuration, (g-i) depict straight configuration, and (j-l) depict bicuspid configuration. Black star denotes inferior semilunar fissure

Table 1.

Configurations as present in different patients

	Question mark	Straight	Single cusp	Bicuspid
Configuration in cut section	14	12	7	1
Configuration in MRI	42	43	18	2
Configuration in patients	8	9	3	1

MRI - Magnetic resonance imaging

In question-mark and bicuspid variants, the inferior semilunar fissure separating the cerebellar tonsils from the rest of the cerebellum coincided with the caudal border of the superior cusp in all 22 specimens. There was no discernible surface landmark for the inferior semilunar fissure in 20 cases where there was either a straight configuration or a single cusp configuration of the occipital bone.

Magnetic resonance imaging sagittal sections

Following the study of anatomical relations in sagittal cut sections of the skull, a study of 105 sagittal T1W images of normal individuals was done. The configuration of the occipital bone and relation of the marrow cavity to the inferior semilunar fissure seen in cut sections corresponded to the relation and anatomy of these structures in MRI sections. Of the 105 individuals studied, bone showed a single cusp-like configuration in 18 specimens. The occipital bone showed the “question-mark” configuration in 48 individuals. The straight configuration with no cusp was seen in 36 individuals, whereas 3 of the individuals showed a bicuspid configuration [Figure 1 and Table 1].

In congruence with the study of the cut sections, in the question-mark variant, the inferior semilunar fissure separating the cerebellar tonsils from the rest of the cerebellum coincided with the caudal border of the superior cusp in all individuals.

The marrow cavity of the occipital bone extended till the same plane as the semilunar fissure in 87 individuals regardless of the configuration of the bone. In 13 individuals, the marrow cavity ended slightly before it reached the same plane as the inferior semilunar fissure, and in 4, it extended beyond.

Patient demographics and clinical features

In total, 27 patients underwent FMD during this study. As 6 patients had follow-up less than 6 months, they were excluded from the study. Of the remaining 21 patients, 13 were female, and 8 were male. The mean age of the patients was 27.83 ± 34 years. Among 21, 12 patients had syrinx at the time of presentation. Of these, 8 had cervicothoracic syrinx, whereas 4 had multi-level syrinx. The most common cause of presentation was headache (14 patients), whereas sensory deficits were the cause of presentation in eight patients. However, on clinical examination, 6 other patients had sensory deficits. Six patients had motor deficits, and 5 had scoliosis [Table 2].

Table 2.

Clinical features of patients in preoperative and follow-up phase

Clinical feature	Preoperative	At last follow-up
		Resolved	Improved	Static
Syrinx	12	4	8
Cervicothoracic	8	4	4	0
Multi-level	4	0	4 (cervicothoracic syrinx resolved in 1 patient of multi-level syrinx)
Sensory	14 (8+6)		14	0
Headache	14	9	5	0
Motor	6	0	2	4
Scoliosis	5	0	0	4

Radiological landmarks

We found that of the 21 patients, the surface anatomical landmarks studied in cut sections were still valid despite the anomalous posterior fossa anatomy in Chiari I malformation. Bicuspid anatomy of the occipital crest was seen in one of the patients out of 21, whereas question-mark anatomy was seen in eight patients, and straight bone anatomy in six patients. Three patients had a single cusp variant. MRI of all 10 patients with bicuspid or question-mark configuration showed that the inferior semilunar fissure coincided with the junction of the superior cusp with the inferior cusp or the straight line, respectively. In all patients, the inferior semilunar fissure invariably coincided with the end of the marrow cavity [Table 1].

Operative features

In each of the patients, the decompression of the occipital bone was earmarked to be limited such that it did not cross the vertical line drawn passing through the inferior semilunar fissure [Figure 2]. The limits of decompression based on proposed parameters were found to be 2 cm × 2 cm for 12 patients, 2.5 cm × 2.5 cm for four patients, and 3 cm × 3 cm for five patients. In one patient, there was an inadvertent breach of the limits thus calculated, and the final bony decompression was 2 cm × 2.5 cm. In this patient, the dural incision was kept limited to previously decided boundaries, and the dura was “firmed up” using coagulation.

Figure 2.

Diagrammatic representation of decompression to be performed in each of the four configurations (a) question-mark, (b) single cusp, (c) straight, and (d) bicuspid. Black star marks inferior semilunar fissure, dark shading denotes tonsils, red vertical line demarcates the boundaries of decompression, and the extent of decompressed bone is shown by transparent red shading

Follow-up

On follow-up imaging at 6 months postoperatively, the syrinx had completely resolved in four patients, whereas in the other eight patients, there was a regression of the syrinx. Of the four patients with multi-level syrinx, one had complete resolution of cervical syrinx with regression of thoraco-lumbar syrinx while the other 3 had regression of all syrinxes but complete resolution of none.

Of the 14 patients with headache, 9 had complete resolution of headache, 4 had near total resolution while one patient complained of occasional bouts of headache compared to a persistent headache present preoperatively.

Sensory deficits had resolved to near normalcy in all patients, though none had complete resolution of symptoms or signs. Similarly, motor deficits had improved in 2 of the six patients and had remained static in the rest. Scoliosis had showed no resolution at 6 months in any of the five patients.

None of the patients showed clinical or radiological signs of cerebellar ptosis [Table 2]. An illustrative image along with imaging of a patient who had cerebellar ptosis due to excessive decompression, is shown in Figure 3.

Figure 3.

(a) A patient with Chiari I Malformation with cervicothoracic syrinx marked with thin white arrows. (b) Postoperative image of the same patient at 6 months follow-up showing regression of syrinx marked with thin black arrows. The extent of bony decompression is marked with a broad white arrow. (c) Postoperative image of another patient who underwent wide decompression, marked by a broad white arrow, and had cerebellar slump with pseudomeningocele marked by a white 4-point star. Red 5-point star marks the inferior semilunar fissure

DISCUSSION

In 1891, Hans Chiari described an entity which is known today as Chiari type I malformation (CM-I).[1] It is widely accepted that CM-I results from a mesodermal defect leading to a small, underdeveloped posterior fossa. Because the cerebellum continues to enlarge after birth, a herniation of the tonsils results. The herniation may provoke a vicious cycle wherein it causes obstruction to the normal CSF pathway that will contribute to further descent.

Considerable variation exists in the position of the cerebellar tonsils in the normal population, and the position may change with age.[9,10] Barkovich et al. recommend the lowest normal position of the cerebellar tonsils to be 3 mm below the foramen magnum with a specificity of 99.5%, although Milhorat et al. hold that the position of the tonsils alone should not exclude the diagnosis.[11,12]

The Chiari I malformation may be associated with a number of other anomalies, including that of CVJ. These may include spina bifida defects, hydrocephalus, or atlanto-axial instability and basilar invagination.

The guidelines on treatment strategy, optimal timing, and optimal technique remain equivocal.[13,14,15] The traditional standard surgical treatment for the Chiari I malformation is considered to be sub-occipital decompression. A significant development in the surgical management of Chiari malformation has been advanced by Goel that atlantoaxial instability is frequently the underlying cause of Chiari I malformation, even when conventional radiologic findings of instability are absent.[2] Goel’s proposition has been substantiated in multiple clinical series, including both adult and pediatric populations, wherein patients underwent C1-C2 stabilization with reported improvements in symptoms and radiological resolution of syringomyelia.[2,16,17,18,19] This theory represents a major conceptual shift from the traditional pathophysiological model of tonsillar herniation secondary to posterior fossa crowding, suggesting instead that “central” or occult instability at the craniovertebral junction plays a direct etiological role.

While outcome data from Goel’s procedure support the safety and potential benefits of this approach, the generalizability and precise indications for C1-C2 fixation in Chiari malformation remain subjects of ongoing debate.[20,21] Until these concepts are more widely validated and incorporated into standard management algorithms, FMD remains the cornerstone of treatment.[3]

As regards the sub-occipital decompression involving an FMD coupled with, in various combinations, excision of the posterior arch of atlas, durotomy, an expansile duroplasty, resection of tonsils, and release of dural or arachnoid adhesions, there remains a want of consensus on nuances such as the necessity for durotomy or resection of the cerebellar tonsils.[13,15,22,23,24,25,26] In fact, Goel et al. have advocated at one time that bony decompression alone may suffice.[27]

Whatever the surgical steps, these surgeries have their own share of complications, such as CVJ instability, scar formation, and consequent stenosis of the CSF outflow, pseudomeningocele formation, and CSF leak.[28,29] There may be a persistent headache due to adhesion of nuchal musculature to dura.[28,29] Another complication of the procedure that has received comparatively less attention is cerebellar ptosis or cerebellar slump, first described by Williams in 1978 in a young woman who suffered from a new onset of severe headache after having undergone a wide sub-occipital craniectomy.[4] It is presumed that the cerebellum settles into the bony defect and can cause a new obstruction to CSF flow in the region of the cisterna magna and may led to nonresolution or enlargement of syrinx and headache, especially in the trigeminal distribution. The cause of the aforementioned cerebellar ptosis or slump is a decompression “that is too large for the specific patient.”[30]

The size of the optimal craniectomy for Chiari I malformation remains as varied as the number of authors describing it.[31] Dewaele insists that it remains difficult to tailor the craniectomy to the correct size.[32] Small craniectomies (<3 cm) can result in an insufficient release of CSF, while large craniectomies (>4 cm) can result in cerebellar ptosis. In their description of two cases, an extensive craniectomy (3.5 cm × 6 cm) caused the extreme cerebellar slump in one case, whereas a small decompression (2 cm × 2 cm) could not prevent an acute, almost lethal ptosis.[32] Most authors, however, do warn against extensive decompression. Klekamp et al. found a significant improvement in results following a smaller craniectomy.[33] Duddy and Williams stated that the herniation of the cerebellar structures and brainstem, as observed in the postoperative period, is attributed to a large craniectomy.[6] Navarro et al. maintain that decompression should be tailored to match the size of the normal cisterna magna, implying a decompression of 3 cm².[34] Incidentally, cerebellar ptosis has also been reported if duroplasty is not performed after durotomy.[5]

Contrarily, Sahuquillo et al. and da Silva et al. advocate an extensive craniectomy with formation of an artificial cisterna magna.[35,36] Interestingly, they noted an upward migration of the cerebellum after such large craniectomies. Vanaclocha et al. also noted an ascent by 4.3 mm after extensive bone removal.[37]

Galarza et al. presented a “Triple R” technique in which the bone resection is limited to the occipital rim of the foramen magnum, followed by selective reposition, reduction, or resection of herniated cerebellar tonsils. This technique straddles the line between decompression and tonsillar “manipulation.”[38]

A number of techniques have been proposed to address the problem of cerebellar ptosis. Williams himself thought that the only treatable condition following slump was hydrocephalus and reiterated that “… if there is no hydrocephalus, there seems little to do.”[4,24] Other authors have proposed cranioplasty and strengthening of dural support. Dewaele et al. have suggested the reverse Trendelenburg position for treatment of symptoms of cerebellar slump and reconstitution of bony support after resolution of symptoms.[32] There have also been recommendations to use pericranium as material for dural graft, as other substitutes tend to lose strength over time and thus predispose to cerebellar ptosis.

We propound that the inconsistency of the results achieved by various authors may in part be due to the attempt to define the boundaries of decompression in absolute numbers. It may be borne in mind that the posterior fossa anatomy in these patients is anomalous, the posterior fossa is classically “small” to varying degrees, and the amount of tonsillar herniation and distortion of cerebellar mechanics is variable. We propose that the decompression be tailored to individual patients. We also proposition that it is the “cramming up” of the essentially pedunculated tonsils that results in CSF outflow obstruction and consequent features of Chiari I malformation, and cerebellar bulk has little contribution to the effect.

On the contrary, a decompression that renders the cerebellum devoid of its bony and dural hammock will allow the cerebellum to migrate anteriorly and inferiorly. The resultant drag on the posterior fossa structures can, to various extents, create a new obstruction to CSF dynamics and render the surgery not only futile but may even cause an appearance of new complications, such as cerebellar ptosis.

In fact, the overall plethora of postoperative complications such as pseudomeningocoele, failure of symptoms to improve or that of syrinx to resolve and appearance of new clinical features due to cerebellar ptosis may be comprehended well if we were to consider them a continuous spectrum of features that result from varying degrees of cerebellar migration, from occult to overt, consequent to loss of cerebellar “hammock.”

Hence, the aforementioned individually tailored decompression should be such that the bulk of cerebellum constituted by the hemispheres remains supported postoperatively by the cusp of occipital bone, while at the same time the tonsils are rendered free of their constraints. This may be achieved by a careful study of the imaging and measuring the distance of the inferior semilunar fissure from the lip of the foramen magnum which corresponds to the end of the marrow cavity on bone.

In our series, all patients underwent decompression after careful calculation of the required size of decompression based on anatomical landmarks. This allowed us to tailor the size of decompression to individual patients and thus achieve optimal decompression without compromising support for the cerebellum. None of our patients had symptoms of cerebellar slump while at the same time, they had good resolution of symptoms, including regression or resolution of syrinx.

Limitations

There are quite a few limitations of our present study.

Though the principle of decompression limits in our study is based on the study of a fair number of skull cut-sections and MRI sagittal images, we recognize that this patient group is small and results may not be representative. Larger study groups, coupled with advanced modalities of study such as cine-MRI, are needed to better understand the CSF dynamics following such decompression.

In addition, symptoms of nonimprovement and cerebellar ptosis itself can be vague and ill-defined, making the clinical symptoms difficult to relate to what is seen on MRI.

The present study has no direct comparison to results from other techniques or a control group, which may make the argument for the superiority of this technique less convincing. It may be argued that perhaps one could decompress the past semilunar fissure with good results as well. Furthermore, the landmarks have been defined only in sagittal anatomy. Decompression of the foramen magnum includes lateral decompression, which was not considered in the present study as a separate entity. We’d like to emphasize again that the semilunar fissure was postulated to be the limit based on an anatomic-biomechanical understanding of the region. While the precise limits will require a study with control groups and direct comparison of techniques, we feel the landmark defined by us marks an optimal point between “too little” and “too much.” In addition, it is more important to realize that the decompression needs to be individualized.

As such, we do believe that the results in themselves constitute a sufficient “proof-of-concept.”

CONCLUSION

The size of bony decompression for Chiari I malformation should be tailored to individual patients to correspond to inferior semilunar fissure so as to achieve optimal decompression and prevent complications of cerebellar ptosis. This may be achieved by identifying the landmarks on imaging as delineated.

Conflicts of interest

There are no conflicts of interest.

Funding Statement

Nil.