Clinical Anatomy 28:683–689 (2015)
ORIGINAL COMMUNICATION
Biomechanical Effects of the Transcondylar Approach on the Craniovertebral Junction ALBERTO C. CARDOSO,1 RICARDO B.V. FONTES,2* LEE A. TAN,2 ALBERT L. RHOTON Jr.,3 SUNG W. ROH,4 AND RICHARD G. FESSLER2 1
~ o Paulo, Brazil DFV Neuro, Sa Department of Neurosurgery, Rush University Medical Center, Chicago, Illinois 3 Department of Neurological Surgery, University of Florida, Gainesville, Florida 4 Department of Neurosurgery, Asan Medical Center, University of Ulsan, Seoul, Korea 2
The transcondylar variation of the far-lateral, retrosigmoid approach is intended for pathologies in the anterolateral portion of the foramen magnum. That area is more clearly visualized when a fraction of the ipsilateral occipital condyle is removed. In this study, the biomechanical effect of this approach on occiput-C2 rotation was investigated. Our hypothesis was that the biomechanical characteristics are significantly altered following the transcondylar approach. Five human cadaveric upper cervical spine specimens (occiput-C7) were used in the study. Torsional moments were applied from zero to a maximum of 1.5 N m to the left and to the right using a mechanical testing machine. The resulting rotational motions of the O–C1, C1–2, and O–C2 segments were measured in the intact specimen and after a simulated right-sided transcondylar approach with resection of 2/3 of the condyle, confirmed by CT scanning and visual inspection. After the posterior two-thirds of the occipital condyle were removed, the neutral zone (NZ) increased 1.3 to the left and 2 to the right at C0–C1, and 7.4 to the left and 6.2 to the right at C1–2. The cumulative increase in NZ between O and C2 was 8.7 to the left and 8.2 to the right. The transcondylar approach also resulted in significant increases in range of motion (ROM) in axial rotation to both sides in all segments. ROM increased 2.8 to the left and 2.4 to the right between C0 and C1, 7.3 to the left and 5.4 to the right between C1 and C2, and 10.1 to the left and 7.8 to the right between CO and C2. Upon inspection, the area of the occipital condyle where the alar ligament attaches had been completely removed in three of the five specimens. Removing the posteromedial two-thirds of one occipital condyle alters the normal axial rotational movements of the craniovertebral junction on both sides. The insertion of the alar ligament can be inadvertently removed during condylar resection, and this could contribute to atlanto-axial instability. There is a biomechanical substrate to craniocervical instability following a transcondylar approach; these patients may need to be followed over several years to ensure it does not progress and necessitate occipito-cervical fusion. Clin. Anat. 28:683–689, 2015. VC 2015 Wiley Periodicals, Inc. Key words: atlanto-occipital joint; atlanto-axial joint; anatomy; neurosurgery; range of motion; articular; foramen magnum
*Correspondence to: Ricardo B. V. Fontes, MD, PhD, Department of Neurological Surgery, Rush University Medical Center, 1725 W Harrison, Suite 855, Chicago, IL 60612, USA. E-mail: [email protected]
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2015 Wiley Periodicals, Inc.
Received 10 February 2015; Revised 10 March 2015; Accepted 16 March 2015 Published online 23 April 2015 in Wiley Online (wileyonlinelibrary.com). DOI: 10.1002/ca.22551
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INTRODUCTION Lesions of the lower clivus and anterior portion of the foramen magnum represent a significant surgical challenge; the task of surgically removing them is technically demanding and can entail significant morbidity and even mortality (Wen et al., 1997). The transcondylar approach is an extension of the basic retrosigmoid approach: a unilateral suboccipital craniotomy and removal of at least half of the C1 posterior arch exposes the dura covering the posterior fossa and sigmoid sinus. Further removal of the posteromedial aspect of the occipital condyle enhances access to the anterior part of the foramen magnum while minimizing retraction of neural structures (Seyfried and Rock, 1994; George and Lot, 1995; Al-Mefty et al., 1996; Sen, 1996; Katsuta et al., 1997; Wen et al., 1997). This approach has become increasingly popular since the 1980s; technical advances such as the ultrasonic aspirator and high-speed drills, and increased awareness of the intricate anatomy of this region, have made the procedure safer and, consequently, more common. On the other hand, neurosurgeons have always been aware of the risk of occipito-cervical instability when drilling the occipital condyle. This risk becomes greater when more than the posteromedial two-thirds are exposed, but there is significant debate as to when patients should be prophylactically stabilized based on the amount of occipital condyle that is resected (Shekar and Sen, 1991; Lang et al., 1993; Sen, 1996). We are aware of only one article to date that describes biomechanical alterations following removal of the occipital condyle (Dvorak et al., 1988; Vishteh et al., 1999). Therefore, in this study we used a simulated far-lateral approach to quantify the effects of removing the posteromedial two-thirds of the occipital condyle upon O–C1 and C1–2 rotation, using a slightly different model. Our hypothesis was that biomechanical characteristics are significantly altered following this approach.
MATERIAL AND METHODS Five human cadaveric occipito-cervical specimens were used in this study. IRB approval was waived since the specimens were part of an anatomical collection. There were two female and three male donors with an average age of 62 years (range, 48–72 years). A single occiput-C7 block was removed from a fresh human cadaver at the time of autopsy, sealed in double plastic bags and frozen at 220 C for later use. The specimens were examined radiographically to check for congenital abnormalities and only ageappropriate degenerative changes were found. At the time of the experiment, the specimens were thawed to room temperature and soft tissues were removed including the paraspinal muscles; the craniocervical junction ligaments, articular capsules, and facet joints were left intact. The specimen was secured to a wood block cranially and to a plastic tube of appropriate diameter caudally with Steinmann pins and Plaster of Paris (Fig. 1). Each prepared specimen
Fig. 1. A: Posterior view of the prepared specimen. B: Anterolateral view of the specimen with transducer in place, secured to the lateral masses of C1 and body of C2. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
was then placed in a MTS Bionix 858 servohydraulic mechanical testing machine (MTS Systems Corp., Minneapolis, MN) with both axial and torsional control. Torsional moments were applied from zero to a maximum of 1.5 N m to the left and to the right. This maximum moment was chosen on the basis of literature data known to produce motion in the physiological range without injuring cadaveric spine specimens (Crisco et al., 1991; Barros Filho et al., 1993). An intersegmental motion device, which can dynamically measure planar spinal kinematics, was secured in place by screws to the anterior portion of the clivus, lateral mass of C1, and body of C2 without violating the articular joints. The rotational motion between the segments could then be measured with a displacement transducer. Data from this transducer and a potentiometric goniometer were collected and analyzed using a computerized data acquisition system. These two types of data could then be combined to convert the recorded linear occipito-atlantal (C0–C1) and atlanto-axial (C1–C2) displacements to angular measurements. To obtain repeatable load–displacement curves, each specimen was preconditioned with five load/ unload cycles. On the fifth cycle, the motion was recorded. A schematic representation of the recorded load displacement test is shown in Figure 2; rotational motion of the segments is reported at applied torques of 0.5, 1.0, and 1.5 N m. The neutral zone (NZ) represents the range of motion over which displacement creates zero-load, measured from the neutral position. The elastic zone (EZ) is the displacement from the last zero-load point to the maximum-load point. Range of motion (ROM) is the total angular measurement from the neutral position to the maximum-load point. After each specimen had been tested in the intact state, a simulated transcondylar approach was created on the right side. Two-thirds of the posterior aspect of the right occipital condyle was removed with
O–C2 Rotation After Transcondylar Approach
Fig. 2. Schematic representation of the load–displacement model under which all specimens were tested. EZ, elastic zone; NZ, neutral zone; ROM, range of motion.
a high-speed drill. The specimen was then tested in this “post-operative” state as previously described. Each specimen was subjected to a computer tomography scan (CT) with sagittal reconstruction in both the pre- and post-surgery states to confirm the amount of occipital condyle removed. Finally, the specimens were dissected to assess the integrity of the alar ligament and its condylar insertion qualitatively.
RESULTS CT scanning confirmed resection of the posterior 2/3 of the right occipital condyle in all specimens (Fig. 3). After the biomechanical testing, inspection revealed that in three specimens the area of the occipital condyle where the alar ligament was attached had been completely removed, thus rendering it incompetent. The pre- and post-operative torque–displacement curves are presented in Figure 4. In general, all
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curves were nonlinear. In the O–C1 segment, NZ displacement was minimal in the intact specimen but was greater in the post-operative state for both ipsiand contra-lateral rotations (Fig. 4A). Torque–displacement dynamics was similar, as demonstrated by the shape of the curve in the EZ, but motion was increased on both sides; although it still remained under five degrees postoperatively, ROM was almost twice that of an intact specimen. These changes reached statistical significance at all measured points for ipsilateral (right) rotation. On the other hand, C1– 2 rotation occurred predominantly in the NZ. Following the transcondylar approach, NZ and ROM increased for both right and left rotations, reaching statistical significance at all points for ipsilateral rotation. As expected, when data from the combined O–C2 segment were analyzed, almost all of the rotation occurred at C1–2. Similarly, postoperative changes were more significant in the same segment (Figs. 4B and 4C). Table 1 presents the mean rotation values obtained during testing in the NZ and at maximum applied torque.
DISCUSSION Anatomical Considerations The craniovertebral junction is a funnel-shaped region formed by the occipital bone, atlas, and axis vertebrae. Its unique anatomical characteristics allow more mobility in all three planes than at any other area of the spine. The occipito-atlantal articulation is a horizontal, cup-shaped synovial joint between the occipital condyles and superior articular facets of C1. The configuration of this joint allows motion in the sagittal and coronal planes but little rotation. On the other hand, two groups of synovial joints constitute the atlanto-axial articulation—a medial group of synovial joints between the dens and anterior arch of C1 and a lateral group between the articular facets of C1
Fig. 3. Pre- (A) and post-operative (B) axial computed tomography scans demonstrating removal of the posteromedial two-thirds of the right occipital condyle, as in a far-lateral approach to the foramen magnum. Each measurement unit equals 1 cm.
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Cardoso et al. TABLE 1. Average Pre- and Postoperative Range of Motion (degrees) in the Neutral Zone (NZ) and at Maximum Applied Torque (1.5 N m) Left NZ
1.5 N m
Right NZ
1.5 N m
O–C1 Preoperative Postoperative
20.59 21.86*
22.57 25.36*
0.69 2.68*
2.48 4.88*
C1–2 Preoperative Postoperative
218.16 225.58*
230.84 238.18
18.94 25.12*
34.84 40.26*
O–C2 Preoperative Postoperative
218.75 227.44*
233.41 243.54
19.63 27.80*
37.32 45.14*
*Indicates a statistically significant difference at the .05 level for the pre- versus postoperative comparison.
longitudinal component. They extend from the medial surface of the C1 lateral mass to the same points on the contralateral sides, posterior to the dens. The transverse ligaments thus prevent anterior subluxation of the atlas and provide an axis of rotation for the atlas and skull about the dens. Other ligamentous structures include the tectorial membrane and the apical ligament. The tectorial membrane is a continuation of the posterior longitudinal ligament of the spine, forming a dense band from the posterior vertebral body of the axis to the clivus. It is therefore most important for resisting flexion and extension. Finally, the apical ligament extends from the tip of the dens to the anterior margin of the odontoid process, and has little importance for the stability of the CVJ.
Fig. 4. Torque–displacement curves for the O-C1 (A), C1-2 (B), and O-C2 (C) segments. Error bars represent standard deviation, and asterisks statistical significance at the 0.05 level. Positive values indicate movement to the right (ipsilateral to approach side).
and C2 (Fig. 5). The anatomy of this complex permits a very large amount of motion in the axial plane, a small amount in the sagittal plane and a minimal amount in the coronal plane (Papadopoulos, 1993). Owing to the absence of intervertebral disks in this segment, normal motion and stability depend exclusively upon the integrity of bones, ligaments, and synovial capsules. Functionally, the most important ligaments are the alar and transverse ligaments. The alar ligaments are two strong bands on each side of the cranial part of the dens that extend obliquely to the medial surfaces of the ipsilateral occipital condyle. They have been traditionally assigned the role of rotatory stabilizers of the CVJ. The transverse ligaments correspond to the thick, strong transverse portion of the cruciate ligament, which also contains a
Fig. 5. Posterior view of the foramen magnum, dens, and C2 vertebral body of one of the specimens. This specimen was injected with colored silicone following the experiment and the occiput, posterior arch of C1, transverse ligament, brainstem, and cord were removed. Alar ligaments (arrows) are demonstrated, extending from the lateral aspect of the tip of the dens to the medial surface of the occipital condyle (*). C1 lateral mass is also demonstrated (**). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
O–C2 Rotation After Transcondylar Approach
Fig. 6. Final exposure afforded by a right far-lateral approach. Posterolateral view of the CVJ following a retromastoid craniotomy, resection of the posterior arch of C1 and opening of the dura. The mastoid is marked by an asterisk. The posterior part of the occipital condyle was resected and the vertebral artery mobilized to allow visualization anterior to the brainstem. Cranial nerves VII through XII and the posterior inferior cerebellar and anterior inferior cerebellar arteries are visible. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
Biomechanical and Clinical Considerations There is no “set recipe” for a far-lateral approach to reach lesions in the anterior part of the foramen magnum. The basic far-lateral approach involves dissection of the posterolateral muscles of the CVJ and early identification of the vertebral artery in the C1 foramen transversarium. A suboccipital craniotomy is performed in the retromastoid area, and the ipsilateral half of the posterior C1 arch is removed. Additional anterior exposure can be afforded by resecting part of the occipital condyle. Finally, the exposure is completed by mobilizing the vertebral artery from the foramen transversarium and its dural insertion (Fig. 6) (Wen et al., 1997). Several authors have studied different degrees of condylar resection and the resulting exposure; more anterior exposure can be afforded by additional removal of the condyle (Zhang et al., 2011). While the priority is obviously to minimize
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neural element retraction, and as much condyle as necessary will be resected to achieve this goal, the surgeon could have reasons other than potential cranio-cervical instability for keeping condylar resection to a minimum; two such reasons are concern for working in a deep location with a high-speed drill around important neurovascular structures, and the additional time required in an already prolonged operation. Therefore, each surgery will be unique and there are descriptions of “far-lateral” variations with no condylar resection (so-called “retrocondylar”) or with removal of onethird, one-half, two-thirds or even the complete condyle. Ultimately, patient- and pathology-specific factors such as anatomy and size are the primary determinants of the degree of resection (Bertalanffy and Seeger, 1991; Sen and Sekhar, 1991, 1993; Hakuba and Tsujimoto, 1993; Kratimenos and Crockard, 1993; Lang et al., 1993; Babu et al., 1994; Hosoda et al., 1994; Tedeschi and Rhoton, 1994; Arnold and Sepehrnia, 1995; Katsuta et al., 1997; Wen et al., 1997). The injury model used in this study could effectively replicate a far-lateral transcondylar approach, as shown by the post-procedure CT scans. This model also demonstrated that the surgeon could partially or completely disrupt the insertion of the alar ligament in a significant fraction of cases. Post-procedure, there were significant increases in both NZ and ROM for axial rotation between C0 and C1, C1 and C2, and C0 and C2 for both ipsi- and contra-lateral rotations. While in absolute terms the biggest alterations in stability were seen at C1–2, in relative terms the increase was more significant at O–C2. Furthermore, almost all of the increase in ROM resulted from changes while still in the NZ and not under maximum load. For example, the ROM at C1–2 was increased by 7.4 to the left and 6.18 to the right, but this corresponded to increases of 41 and 33%, respectively, at O–C2. On the other hand, an NZ increase at O–C1 of 1.3 to left and 2 to the right corresponded to increases of 217% and 288%. Certain authors have assumed that unilateral section of the alar ligament would only affect rotation ROM in one direction, but our results support the findings of Panjabi et al. with experimental section of the alar ligament, leading to the increase in rotation ROM in both directions (Dvorak et al., 1987a; Panjabi et al., 1991). Our model differs from that of Panjabi et al. in that this was not a purely experimental “model” injury but an attempt to replicate a surgical approach, so there could have been additional disruption of the O–C1 joint and the posterior atlanto-occipital membrane (Dvorak et al., 1987b; Panjabi, 1992a). Whereas the concept of ROM is fairly straightforward, the NZ is frequently overlooked in biomechanical studies. The NZ is the component of the physiological ROM associated with significant flexibility and minimal stiffness at low loads, while the rest of the physiological ROM is the EZ. It also appears to be the most clinically important measure of spinal stability, increasing with injury of the spinal column and its ligaments (Panjabi, 1992a,b). Stabilization during movement within the NZ in the normal individual is largely influenced by the action of the supporting musculature. Therein lies one of the biggest
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drawbacks of this (and any other) cadaveric study, since it does not take the action of the musculature into account (Panjabi et al., 1991). Data on craniocervical biomechanical properties following a farlateral approach are scarce in the literature. The biomechanical study that most closely resembles the results presented here was published by Vishteh et al. (1999). They performed a more extensive analysis of six cadaveric specimens that included triplanar measurements, perhaps the biggest deficiency in our study. Vishteh et al. (1999) demonstrated increasing ROM with increasing degrees of condylar resection in virtually all three planes. However, the O–C1 changes in the NZ were greater in our study: following a 75% condylectomy, Vishteh et al. (1999) reported an NZ increase of 60.2%, compared to 217–288% here. In addition, they found that stability during ipsilateral rotation was largely maintained, as opposed to our results, which demonstrate a relatively similar effect bilaterally. The reason for this difference is not completely clear to us; Vishteh et al. (1999) did not describe a preconditioning procedure or the number of repetitions utilized in their study and that could explain the difference (Vishteh et al. 1999). Given the reasons outlined above, whether the reported increases in NZ motion and rotation ROM actually result in clinical instability can only be determined in the clinical setting. Vishteh et al. (1999) established a resection threshold of 50%, beyond which ROM values increased significantly, but this is not enough to support a decision to fuse this segment prophylactically, with significant morbidity. General criteria established for O–C2 instability include O–C1 rotation > 8 to each side, O–C1 translation > 1 mm, total lateral displacement of C1–C2 lateral masses > 7 mm, axial rotation C1–C2 > 45 to each side, antero-posterior C1–C2 translation > 4 mm, or radiological evidence of avulsion of the transverse ligament (Panjabi, 1992a). Although our post-injury numbers are near the upper limits of those parameters, absolute numbers to establish limits of instability can mislead because there are large differences in absolute measurements among individuals. However, we have established that a routine transcondylar approach increases those parameters for rotation in a consistent manner to a level significantly different from that of intact specimens. It seems reasonable to assume that O–C1–C2 instability is a reason for persistent neck pain following a retrocondylar approach, particularly if this pain has a dynamic nature or if it is accompanied by transient neurological deficits or progressive deformity. In these patients, surgical stabilization might be an option but so far there are no data to support it in a prophylactic manner following resection of the condyle over a certain threshold. In conclusion, we have demonstrated that a routine transcondylar approach to the anterior foramen magnum that involves resection of the posterior 2/3 of the occipital condyle results in significantly altered biomechanical properties of the craniovertebral junction, thus corroborating the study hypothesis. While these biomechanical parameters are still largely below the upper limit of what is considered normal, instability is a progressive phenomenon and the long-term consequences
of such partial destabilization are unknown. No clinical recommendations should be based solely on a biomechanical study, but special attention should be paid to persistent pain of dynamic nature during the long-term follow-up of these patients as it could indicate subclinical instability finally becoming symptomatic.
ACKNOWLEDGMENTS Authors would like to acknowledge and thank the donors of the cadavers utilized in this study, the University of Florida Tissue Bank, Alachua, Fl., and Ron L. Smith for technical assistance with the manuscript.
REFERENCES Al-Mefty O, Borba LA, Aoki N, Angtuaco E, Pait TG. 1996. The transcondylar approach to extradural nonneoplastic lesions of the craniovertebral junction. J Neurosurg 84:1–6. Arnold H, Sepehrnia A. 1995. Extreme lateral transcondylar approach. J Neurosurg 82:313–314. Babu RP, Sekhar LN, Wright DC. 1994. Extreme lateral transcondylar approach: Technical improvements and lessons learned. J Neurosurg 81:49–59. Barros Filho TE, Oliveira RP, Grave JM, Taricco MA. 1993. Corpectomy and anterior plating in cervical spine fractures with tetraplegia. Rev Paul Med 111:375–377. Bertalanffy H, Seeger W. 1991. The dorsolateral, suboccipital, transcondylar approach to the lower clivus and anterior portion of the craniocervical junction. Neurosurgery 29:815–821. k J, Grob D. 1991. Crisco JJ III, Oda T, Panjabi MM, Bueff HU, Dvora Transections of the C1-C2 joint capsular ligaments in the cadaveric spine. Spine 16:S474–S479. Dvorak J, Hayek J, Zehnder R. 1987a. CT-functional diagnostics of the rotatory instability of the upper cervical spine. II. An evaluation on healthy adults and patients with suspected instability. Spine 12:726–731. Dvorak J, Panjabi M, Gerber M, Wichmann W. 1987b. CT-functional diagnostics of the rotatory instability of upper cervical spine. I. An experimental study on cadavers. Spine 12:197–205. Dvorak J, Schneider E, Saldinger P, Rahn B. 1988. Biomechanics of the craniocervical region: The alar and transverse ligaments. J Orthop Res 6:452–461. George B, Lot G. 1995. Anterolateral and posterolateral approaches to the foramen magnum: Technical description and experience from 97 cases. Skull Base Surg. 5:9–19. Hakuba A, Tsujimoto T. 1993. Transcondylar approach for foramen magnum meningiomas. In: Sekhar LN, Janecka IP, editors. Surgery of cranial base tumors. New York: Raven Press. p 671–678. Hosoda K, Fujita S, Kawaguchi T, Yamada H. 1994. A transcondylar approach to the arteriovenous malformation at the ventral cervicomedullary junction: Report of three cases. Neurosurgery 34: 748–752. discussion 752–753. Katsuta T, Rhoton AL Jr, Matsushima T. 1997. The jugular foramen: Microsurgical anatomy and operative approaches. Neurosurgery 41:149–201. discussion 201–202. Kratimenos GP, Crockard HA. 1993. The far lateral approach for ventrally placed foramen magnum and upper cervical spine tumours. Br J Neurosurg 7:129–140. Lang DA, Neil-Dwyer G, Iannotti F. 1993. The suboccipital transcondylar approach to the clivus and cranio-cervical junction for ventrally placed pathology at and above the foramen magnum. Acta Neurochir (Wien) 125:132–137. Panjabi MM. 1992a. The stabilizing system of the spine. Part I. Function, dysfunction, adaptation, and enhancement. J Spinal Disord 5:383–389. discussion 397.
O–C2 Rotation After Transcondylar Approach Panjabi MM. 1992b. The stabilizing system of the spine. II. Neutral zone and instability hypothesis. J Spinal Disord 5:390–396. discussion 397. Panjabi M, Dvorak J, Crisco JJ III, Oda T, Wang P Grob D. 1991. Effects of alar ligament transection on upper cervical spine rotation. J Orthop Res 9:584–593. Papadopoulos S. 1993. Biomechanics of the occipito-atlanto-axial trauma. In: Rea GL, Miller CA, editors. Spinal Trauma: Current evaluation and Management. American Association of Neurological Surgeons. p 17–24. Sen C. 1996. The transcondylar approach to the lower clivus, foramen magnum and C1-C2. Clin Neurosurg 43:113–126. Sen CN, Sekhar LN. 1991. Surgical management of anteriorly placed lesions at the craniocervical junction—An alternative approach. Acta Neurochir (Wien) 108:70–77. Sen C, Sekhar L. 1993. Extreme lateral transcondylar and transjugular approaches. In: Sekhar LN, Janecka IP, editors. Surgery of Cranial Base Tumors. New York: Raven Press. p 289–312.
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Seyfried DM, Rock JP. 1994. The transcondylar approach to the jugular foramen: A comparative anatomic study. Surg Neurol 42:265–271. Shekar L, Sen C. 1991. The dorsolateral, suboccipital, transcondylar approach to the craniocervical junction (comment). Neurosurgery 29:820–821. Tedeschi H, Rhoton AL Jr. 1994. Lateral approaches to the petroclival region. Surg Neurol 41:180–216. Vishteh AG, Crawford NR, Melton MS, Spetzler RF, Sonntag VK, Dickman CA. 1999. Stability of the craniovertebral junction after unilateral occipital condyle resection: A biomechanical study. J Neurosurg 90:91–98. Wen HT, Rhoton AL Jr, Katsuta T, de Oliveira E. 1997. Microsurgical anatomy of the transcondylar, supracondylar, and paracondylar extensions of the far-lateral approach. J Neurosurg 87:555–585. Zhang H, Lan Q, Wang X. 2011. Neuronavigation-based quantitative study of the far-lateral keyhole approach following partial removal of the occipital condyle and jugular tubercle. J Clin Neurosci 18:678–682.
ORIGINAL COMMUNICATION
Biomechanical Effects of the Transcondylar Approach on the Craniovertebral Junction ALBERTO C. CARDOSO,1 RICARDO B.V. FONTES,2* LEE A. TAN,2 ALBERT L. RHOTON Jr.,3 SUNG W. ROH,4 AND RICHARD G. FESSLER2 1
~ o Paulo, Brazil DFV Neuro, Sa Department of Neurosurgery, Rush University Medical Center, Chicago, Illinois 3 Department of Neurological Surgery, University of Florida, Gainesville, Florida 4 Department of Neurosurgery, Asan Medical Center, University of Ulsan, Seoul, Korea 2
The transcondylar variation of the far-lateral, retrosigmoid approach is intended for pathologies in the anterolateral portion of the foramen magnum. That area is more clearly visualized when a fraction of the ipsilateral occipital condyle is removed. In this study, the biomechanical effect of this approach on occiput-C2 rotation was investigated. Our hypothesis was that the biomechanical characteristics are significantly altered following the transcondylar approach. Five human cadaveric upper cervical spine specimens (occiput-C7) were used in the study. Torsional moments were applied from zero to a maximum of 1.5 N m to the left and to the right using a mechanical testing machine. The resulting rotational motions of the O–C1, C1–2, and O–C2 segments were measured in the intact specimen and after a simulated right-sided transcondylar approach with resection of 2/3 of the condyle, confirmed by CT scanning and visual inspection. After the posterior two-thirds of the occipital condyle were removed, the neutral zone (NZ) increased 1.3 to the left and 2 to the right at C0–C1, and 7.4 to the left and 6.2 to the right at C1–2. The cumulative increase in NZ between O and C2 was 8.7 to the left and 8.2 to the right. The transcondylar approach also resulted in significant increases in range of motion (ROM) in axial rotation to both sides in all segments. ROM increased 2.8 to the left and 2.4 to the right between C0 and C1, 7.3 to the left and 5.4 to the right between C1 and C2, and 10.1 to the left and 7.8 to the right between CO and C2. Upon inspection, the area of the occipital condyle where the alar ligament attaches had been completely removed in three of the five specimens. Removing the posteromedial two-thirds of one occipital condyle alters the normal axial rotational movements of the craniovertebral junction on both sides. The insertion of the alar ligament can be inadvertently removed during condylar resection, and this could contribute to atlanto-axial instability. There is a biomechanical substrate to craniocervical instability following a transcondylar approach; these patients may need to be followed over several years to ensure it does not progress and necessitate occipito-cervical fusion. Clin. Anat. 28:683–689, 2015. VC 2015 Wiley Periodicals, Inc. Key words: atlanto-occipital joint; atlanto-axial joint; anatomy; neurosurgery; range of motion; articular; foramen magnum
*Correspondence to: Ricardo B. V. Fontes, MD, PhD, Department of Neurological Surgery, Rush University Medical Center, 1725 W Harrison, Suite 855, Chicago, IL 60612, USA. E-mail: [email protected]
C V
2015 Wiley Periodicals, Inc.
Received 10 February 2015; Revised 10 March 2015; Accepted 16 March 2015 Published online 23 April 2015 in Wiley Online (wileyonlinelibrary.com). DOI: 10.1002/ca.22551
Library
684
Cardoso et al.
INTRODUCTION Lesions of the lower clivus and anterior portion of the foramen magnum represent a significant surgical challenge; the task of surgically removing them is technically demanding and can entail significant morbidity and even mortality (Wen et al., 1997). The transcondylar approach is an extension of the basic retrosigmoid approach: a unilateral suboccipital craniotomy and removal of at least half of the C1 posterior arch exposes the dura covering the posterior fossa and sigmoid sinus. Further removal of the posteromedial aspect of the occipital condyle enhances access to the anterior part of the foramen magnum while minimizing retraction of neural structures (Seyfried and Rock, 1994; George and Lot, 1995; Al-Mefty et al., 1996; Sen, 1996; Katsuta et al., 1997; Wen et al., 1997). This approach has become increasingly popular since the 1980s; technical advances such as the ultrasonic aspirator and high-speed drills, and increased awareness of the intricate anatomy of this region, have made the procedure safer and, consequently, more common. On the other hand, neurosurgeons have always been aware of the risk of occipito-cervical instability when drilling the occipital condyle. This risk becomes greater when more than the posteromedial two-thirds are exposed, but there is significant debate as to when patients should be prophylactically stabilized based on the amount of occipital condyle that is resected (Shekar and Sen, 1991; Lang et al., 1993; Sen, 1996). We are aware of only one article to date that describes biomechanical alterations following removal of the occipital condyle (Dvorak et al., 1988; Vishteh et al., 1999). Therefore, in this study we used a simulated far-lateral approach to quantify the effects of removing the posteromedial two-thirds of the occipital condyle upon O–C1 and C1–2 rotation, using a slightly different model. Our hypothesis was that biomechanical characteristics are significantly altered following this approach.
MATERIAL AND METHODS Five human cadaveric occipito-cervical specimens were used in this study. IRB approval was waived since the specimens were part of an anatomical collection. There were two female and three male donors with an average age of 62 years (range, 48–72 years). A single occiput-C7 block was removed from a fresh human cadaver at the time of autopsy, sealed in double plastic bags and frozen at 220 C for later use. The specimens were examined radiographically to check for congenital abnormalities and only ageappropriate degenerative changes were found. At the time of the experiment, the specimens were thawed to room temperature and soft tissues were removed including the paraspinal muscles; the craniocervical junction ligaments, articular capsules, and facet joints were left intact. The specimen was secured to a wood block cranially and to a plastic tube of appropriate diameter caudally with Steinmann pins and Plaster of Paris (Fig. 1). Each prepared specimen
Fig. 1. A: Posterior view of the prepared specimen. B: Anterolateral view of the specimen with transducer in place, secured to the lateral masses of C1 and body of C2. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
was then placed in a MTS Bionix 858 servohydraulic mechanical testing machine (MTS Systems Corp., Minneapolis, MN) with both axial and torsional control. Torsional moments were applied from zero to a maximum of 1.5 N m to the left and to the right. This maximum moment was chosen on the basis of literature data known to produce motion in the physiological range without injuring cadaveric spine specimens (Crisco et al., 1991; Barros Filho et al., 1993). An intersegmental motion device, which can dynamically measure planar spinal kinematics, was secured in place by screws to the anterior portion of the clivus, lateral mass of C1, and body of C2 without violating the articular joints. The rotational motion between the segments could then be measured with a displacement transducer. Data from this transducer and a potentiometric goniometer were collected and analyzed using a computerized data acquisition system. These two types of data could then be combined to convert the recorded linear occipito-atlantal (C0–C1) and atlanto-axial (C1–C2) displacements to angular measurements. To obtain repeatable load–displacement curves, each specimen was preconditioned with five load/ unload cycles. On the fifth cycle, the motion was recorded. A schematic representation of the recorded load displacement test is shown in Figure 2; rotational motion of the segments is reported at applied torques of 0.5, 1.0, and 1.5 N m. The neutral zone (NZ) represents the range of motion over which displacement creates zero-load, measured from the neutral position. The elastic zone (EZ) is the displacement from the last zero-load point to the maximum-load point. Range of motion (ROM) is the total angular measurement from the neutral position to the maximum-load point. After each specimen had been tested in the intact state, a simulated transcondylar approach was created on the right side. Two-thirds of the posterior aspect of the right occipital condyle was removed with
O–C2 Rotation After Transcondylar Approach
Fig. 2. Schematic representation of the load–displacement model under which all specimens were tested. EZ, elastic zone; NZ, neutral zone; ROM, range of motion.
a high-speed drill. The specimen was then tested in this “post-operative” state as previously described. Each specimen was subjected to a computer tomography scan (CT) with sagittal reconstruction in both the pre- and post-surgery states to confirm the amount of occipital condyle removed. Finally, the specimens were dissected to assess the integrity of the alar ligament and its condylar insertion qualitatively.
RESULTS CT scanning confirmed resection of the posterior 2/3 of the right occipital condyle in all specimens (Fig. 3). After the biomechanical testing, inspection revealed that in three specimens the area of the occipital condyle where the alar ligament was attached had been completely removed, thus rendering it incompetent. The pre- and post-operative torque–displacement curves are presented in Figure 4. In general, all
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curves were nonlinear. In the O–C1 segment, NZ displacement was minimal in the intact specimen but was greater in the post-operative state for both ipsiand contra-lateral rotations (Fig. 4A). Torque–displacement dynamics was similar, as demonstrated by the shape of the curve in the EZ, but motion was increased on both sides; although it still remained under five degrees postoperatively, ROM was almost twice that of an intact specimen. These changes reached statistical significance at all measured points for ipsilateral (right) rotation. On the other hand, C1– 2 rotation occurred predominantly in the NZ. Following the transcondylar approach, NZ and ROM increased for both right and left rotations, reaching statistical significance at all points for ipsilateral rotation. As expected, when data from the combined O–C2 segment were analyzed, almost all of the rotation occurred at C1–2. Similarly, postoperative changes were more significant in the same segment (Figs. 4B and 4C). Table 1 presents the mean rotation values obtained during testing in the NZ and at maximum applied torque.
DISCUSSION Anatomical Considerations The craniovertebral junction is a funnel-shaped region formed by the occipital bone, atlas, and axis vertebrae. Its unique anatomical characteristics allow more mobility in all three planes than at any other area of the spine. The occipito-atlantal articulation is a horizontal, cup-shaped synovial joint between the occipital condyles and superior articular facets of C1. The configuration of this joint allows motion in the sagittal and coronal planes but little rotation. On the other hand, two groups of synovial joints constitute the atlanto-axial articulation—a medial group of synovial joints between the dens and anterior arch of C1 and a lateral group between the articular facets of C1
Fig. 3. Pre- (A) and post-operative (B) axial computed tomography scans demonstrating removal of the posteromedial two-thirds of the right occipital condyle, as in a far-lateral approach to the foramen magnum. Each measurement unit equals 1 cm.
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Cardoso et al. TABLE 1. Average Pre- and Postoperative Range of Motion (degrees) in the Neutral Zone (NZ) and at Maximum Applied Torque (1.5 N m) Left NZ
1.5 N m
Right NZ
1.5 N m
O–C1 Preoperative Postoperative
20.59 21.86*
22.57 25.36*
0.69 2.68*
2.48 4.88*
C1–2 Preoperative Postoperative
218.16 225.58*
230.84 238.18
18.94 25.12*
34.84 40.26*
O–C2 Preoperative Postoperative
218.75 227.44*
233.41 243.54
19.63 27.80*
37.32 45.14*
*Indicates a statistically significant difference at the .05 level for the pre- versus postoperative comparison.
longitudinal component. They extend from the medial surface of the C1 lateral mass to the same points on the contralateral sides, posterior to the dens. The transverse ligaments thus prevent anterior subluxation of the atlas and provide an axis of rotation for the atlas and skull about the dens. Other ligamentous structures include the tectorial membrane and the apical ligament. The tectorial membrane is a continuation of the posterior longitudinal ligament of the spine, forming a dense band from the posterior vertebral body of the axis to the clivus. It is therefore most important for resisting flexion and extension. Finally, the apical ligament extends from the tip of the dens to the anterior margin of the odontoid process, and has little importance for the stability of the CVJ.
Fig. 4. Torque–displacement curves for the O-C1 (A), C1-2 (B), and O-C2 (C) segments. Error bars represent standard deviation, and asterisks statistical significance at the 0.05 level. Positive values indicate movement to the right (ipsilateral to approach side).
and C2 (Fig. 5). The anatomy of this complex permits a very large amount of motion in the axial plane, a small amount in the sagittal plane and a minimal amount in the coronal plane (Papadopoulos, 1993). Owing to the absence of intervertebral disks in this segment, normal motion and stability depend exclusively upon the integrity of bones, ligaments, and synovial capsules. Functionally, the most important ligaments are the alar and transverse ligaments. The alar ligaments are two strong bands on each side of the cranial part of the dens that extend obliquely to the medial surfaces of the ipsilateral occipital condyle. They have been traditionally assigned the role of rotatory stabilizers of the CVJ. The transverse ligaments correspond to the thick, strong transverse portion of the cruciate ligament, which also contains a
Fig. 5. Posterior view of the foramen magnum, dens, and C2 vertebral body of one of the specimens. This specimen was injected with colored silicone following the experiment and the occiput, posterior arch of C1, transverse ligament, brainstem, and cord were removed. Alar ligaments (arrows) are demonstrated, extending from the lateral aspect of the tip of the dens to the medial surface of the occipital condyle (*). C1 lateral mass is also demonstrated (**). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
O–C2 Rotation After Transcondylar Approach
Fig. 6. Final exposure afforded by a right far-lateral approach. Posterolateral view of the CVJ following a retromastoid craniotomy, resection of the posterior arch of C1 and opening of the dura. The mastoid is marked by an asterisk. The posterior part of the occipital condyle was resected and the vertebral artery mobilized to allow visualization anterior to the brainstem. Cranial nerves VII through XII and the posterior inferior cerebellar and anterior inferior cerebellar arteries are visible. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
Biomechanical and Clinical Considerations There is no “set recipe” for a far-lateral approach to reach lesions in the anterior part of the foramen magnum. The basic far-lateral approach involves dissection of the posterolateral muscles of the CVJ and early identification of the vertebral artery in the C1 foramen transversarium. A suboccipital craniotomy is performed in the retromastoid area, and the ipsilateral half of the posterior C1 arch is removed. Additional anterior exposure can be afforded by resecting part of the occipital condyle. Finally, the exposure is completed by mobilizing the vertebral artery from the foramen transversarium and its dural insertion (Fig. 6) (Wen et al., 1997). Several authors have studied different degrees of condylar resection and the resulting exposure; more anterior exposure can be afforded by additional removal of the condyle (Zhang et al., 2011). While the priority is obviously to minimize
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neural element retraction, and as much condyle as necessary will be resected to achieve this goal, the surgeon could have reasons other than potential cranio-cervical instability for keeping condylar resection to a minimum; two such reasons are concern for working in a deep location with a high-speed drill around important neurovascular structures, and the additional time required in an already prolonged operation. Therefore, each surgery will be unique and there are descriptions of “far-lateral” variations with no condylar resection (so-called “retrocondylar”) or with removal of onethird, one-half, two-thirds or even the complete condyle. Ultimately, patient- and pathology-specific factors such as anatomy and size are the primary determinants of the degree of resection (Bertalanffy and Seeger, 1991; Sen and Sekhar, 1991, 1993; Hakuba and Tsujimoto, 1993; Kratimenos and Crockard, 1993; Lang et al., 1993; Babu et al., 1994; Hosoda et al., 1994; Tedeschi and Rhoton, 1994; Arnold and Sepehrnia, 1995; Katsuta et al., 1997; Wen et al., 1997). The injury model used in this study could effectively replicate a far-lateral transcondylar approach, as shown by the post-procedure CT scans. This model also demonstrated that the surgeon could partially or completely disrupt the insertion of the alar ligament in a significant fraction of cases. Post-procedure, there were significant increases in both NZ and ROM for axial rotation between C0 and C1, C1 and C2, and C0 and C2 for both ipsi- and contra-lateral rotations. While in absolute terms the biggest alterations in stability were seen at C1–2, in relative terms the increase was more significant at O–C2. Furthermore, almost all of the increase in ROM resulted from changes while still in the NZ and not under maximum load. For example, the ROM at C1–2 was increased by 7.4 to the left and 6.18 to the right, but this corresponded to increases of 41 and 33%, respectively, at O–C2. On the other hand, an NZ increase at O–C1 of 1.3 to left and 2 to the right corresponded to increases of 217% and 288%. Certain authors have assumed that unilateral section of the alar ligament would only affect rotation ROM in one direction, but our results support the findings of Panjabi et al. with experimental section of the alar ligament, leading to the increase in rotation ROM in both directions (Dvorak et al., 1987a; Panjabi et al., 1991). Our model differs from that of Panjabi et al. in that this was not a purely experimental “model” injury but an attempt to replicate a surgical approach, so there could have been additional disruption of the O–C1 joint and the posterior atlanto-occipital membrane (Dvorak et al., 1987b; Panjabi, 1992a). Whereas the concept of ROM is fairly straightforward, the NZ is frequently overlooked in biomechanical studies. The NZ is the component of the physiological ROM associated with significant flexibility and minimal stiffness at low loads, while the rest of the physiological ROM is the EZ. It also appears to be the most clinically important measure of spinal stability, increasing with injury of the spinal column and its ligaments (Panjabi, 1992a,b). Stabilization during movement within the NZ in the normal individual is largely influenced by the action of the supporting musculature. Therein lies one of the biggest
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drawbacks of this (and any other) cadaveric study, since it does not take the action of the musculature into account (Panjabi et al., 1991). Data on craniocervical biomechanical properties following a farlateral approach are scarce in the literature. The biomechanical study that most closely resembles the results presented here was published by Vishteh et al. (1999). They performed a more extensive analysis of six cadaveric specimens that included triplanar measurements, perhaps the biggest deficiency in our study. Vishteh et al. (1999) demonstrated increasing ROM with increasing degrees of condylar resection in virtually all three planes. However, the O–C1 changes in the NZ were greater in our study: following a 75% condylectomy, Vishteh et al. (1999) reported an NZ increase of 60.2%, compared to 217–288% here. In addition, they found that stability during ipsilateral rotation was largely maintained, as opposed to our results, which demonstrate a relatively similar effect bilaterally. The reason for this difference is not completely clear to us; Vishteh et al. (1999) did not describe a preconditioning procedure or the number of repetitions utilized in their study and that could explain the difference (Vishteh et al. 1999). Given the reasons outlined above, whether the reported increases in NZ motion and rotation ROM actually result in clinical instability can only be determined in the clinical setting. Vishteh et al. (1999) established a resection threshold of 50%, beyond which ROM values increased significantly, but this is not enough to support a decision to fuse this segment prophylactically, with significant morbidity. General criteria established for O–C2 instability include O–C1 rotation > 8 to each side, O–C1 translation > 1 mm, total lateral displacement of C1–C2 lateral masses > 7 mm, axial rotation C1–C2 > 45 to each side, antero-posterior C1–C2 translation > 4 mm, or radiological evidence of avulsion of the transverse ligament (Panjabi, 1992a). Although our post-injury numbers are near the upper limits of those parameters, absolute numbers to establish limits of instability can mislead because there are large differences in absolute measurements among individuals. However, we have established that a routine transcondylar approach increases those parameters for rotation in a consistent manner to a level significantly different from that of intact specimens. It seems reasonable to assume that O–C1–C2 instability is a reason for persistent neck pain following a retrocondylar approach, particularly if this pain has a dynamic nature or if it is accompanied by transient neurological deficits or progressive deformity. In these patients, surgical stabilization might be an option but so far there are no data to support it in a prophylactic manner following resection of the condyle over a certain threshold. In conclusion, we have demonstrated that a routine transcondylar approach to the anterior foramen magnum that involves resection of the posterior 2/3 of the occipital condyle results in significantly altered biomechanical properties of the craniovertebral junction, thus corroborating the study hypothesis. While these biomechanical parameters are still largely below the upper limit of what is considered normal, instability is a progressive phenomenon and the long-term consequences
of such partial destabilization are unknown. No clinical recommendations should be based solely on a biomechanical study, but special attention should be paid to persistent pain of dynamic nature during the long-term follow-up of these patients as it could indicate subclinical instability finally becoming symptomatic.
ACKNOWLEDGMENTS Authors would like to acknowledge and thank the donors of the cadavers utilized in this study, the University of Florida Tissue Bank, Alachua, Fl., and Ron L. Smith for technical assistance with the manuscript.
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