Introduction

The cranio-vertebral junction (CVJ) has long been considered surgically challenging, due to its complex anatomical features that include vital neurovascular structures and to its unique biomechanical properties. Subsequently, high morbidity from short- and long-term complications was accepted and considered inevitable due to the complexity of surgery. However, the concept of “acceptable morbidity” is outdated as a result of surgical evolution, new technology, and patient awareness that provides the means and the expectations toward lesser morbidity in all fields of surgery. Lately, safety of CVJ surgery has increased due to the introduction and implementation of technological advancements, both in imaging and surgical assistance.

Anatomically, CVJ encompasses the occiput (C0) and the first two cervical vertebrae (C1 and C2) and so represents the transition zone between the skull and the mobile cervical spine. Its unique bony-ligamentous configuration allows for complex movements. While the C0-C1 joint is mostly involved in flexion and extension of the head, the C1-C2 joint provides most of the rotation in the cervical spine. Moreover, the configuration and orientation of the condyles and C1-C2 articular processes also enable lateral bending.

Surgically related considerations regarding CVJ anatomy include the following:

  • The sharp angle between the occiput and the upper cervical spine creates a significant lever arm that counteracts surgical fixation devices [6]

  • Space for the application of bone graft is limited compared to the thoracolumbar spine [64]

  • Instrumentation is risk-laden due to the proximity of vascular and neural structures

  • The weight discrepancy, especially in children, between the head and the cervical spine exposes the hardware to high loads and increases the risk of failure

  • The thinness of the occipital bone usually present to the sides of the midline represents a challenge for occipital plating and may impact the hardware’s resistance to loading

  • CVJ is a frequent site of bony and vascular anomalies (e.g., high-riding vertebral artery and os ponticulus) that increase the risk of hardware related complications.

Accordingly, instrumentation and surgical strategies have evolved to obtain more solid constructs while respecting the surrounding vital neurovascular structures. Various novel techniques—radiological, surgical, and technological—have been described in an attempt to enhance surgical efficacy. Here, we review the technological advancements of the last years and their implementation into modern surgical practice. Moreover, we analyzed their contribution to safety and effectiveness in the work-up and the surgical management of the cranio-vertebral junction. A deep knowledge of these novel techniques and of their implementation in clinical routine practice might make CVJ surgery safer and more effective than in the past.

Novelties for safer CVJ surgery

Advancements in technology and knowledge have allowed increasing safety and reproducibility of surgical procedures. Patients harboring traumatic, tumoral, infective, degenerative and malformative lesions of the CVJ require very often complex surgeries that are associated with elevated neurological and functional risks.

Advancements concern imaging, biologics, customized implants and 3D-printed technology, intraoperative computer assistance (e.g., navigation and robotics), video-assisted approaches, and intraoperative neuromonitoring.

This article provides a critical review on the state of the art and the latest technological innovations involving safety in CVJ surgery.

Advancements in diagnostic imaging

Advancements in 3-dimensional (3D) CT-scan reconstruction and MR imaging have led to a better understanding and work-up of ligamentous injuries at CVJ, which, if undetected, might lead to a chronic painful instability [4]. Indeed, in the last decades, the gradual technological improvement has been followed by the introduction of novel diagnostic radiological criteria for atlantooccipital dislocation (AOD), as for example the condylar sum (Fig. 1a–c) [4, 15]. Historically, this life-threatening traumatic injury of the CVJ was diagnosed on X-rays or regular CT-scan. In current practice, MRI has increasingly come to complete this initial osseous radiological assessment by providing a targeted evaluation of the integrity of CVJ’s ligamentous structures [65].

Fig. 1
figure 1

Atlantoaxial dislocation type II. a CT scan, coronal view, showing an increased occipital condyle-C1 interval (red circles). The condylar sum is defined as the sum of a patient’s left and right mean cranio-cervical interval (CCI) values. A distance > 2 mm in adults or > 5 mm in children, or a gross asymmetry between the two C0–C1 joints is highly sensitive and specific for AOD. b CT scan, sagittal view, focusing on basion-dens interval (red line). c CT scan, sagittal view, displaying an increased occipital condyle-C1 interval (red lines). d T2-weighted MRI, sagittal view, pointing out a fluid signal in the atlanto-occipital joint (red circle). e T2-weighted MRI, sagittal view, showing abnormal signal at the basion-dens interval, translating the disruption of the anterior atlanto-occipital membrane (red arrow), apical ligament (dotted red arrow), tectorial membrane (green arrow), and posterior atlantooccipital membrane (green dotted arrow)

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In the current practice, STIR (short tau inversion recovery) sequences are particularly useful in this regard providing direct assessment of stability at the C1–C2 level, with potential implications on the therapeutic approach [68]. The transverse atlantal ligament (TAL) is crucial for C1–C2 instability. X-ray and CT-based measurements, such as the atlantodental interval (distance between posterior aspect of anterior tubercle of C1 and anterior aspect of odontoid peg) and the rule of Spence (where if the combined projection of the lateral masses of the atlas is more than 6.9 mm beyond the lateral masses of the axis, an injury to transverse ligament is likely), have lack of sensitivity [10]. In this scenario, Dickman et al. propose a new classification for TAL injuries based on X-ray, CT, and MR screening. The injuries were classified as disruptions of the substance of the ligament (type I) or as fractures and avulsions involving the tubercle for insertion of the TAL on the C1 lateral mass (type II), with type IA—namely, a central avulsion of the TAL—having no chance of healing under conservative treatment thus requiring fixation [12].

MRI is also useful to assess other ligamentous structures such as the apical and alar ligaments and the tectorial membrane or to identify indirect signs of latent craniovertebral instability in the trauma setting such as facet joint fluid effusion (Fig. 1d) or prevertebral hematomas (Fig. 1e) [65].

Finally, 3D CT-scan reconstruction and multiplanar reformatted (MPR) images provide a comprehensive overview of CVJ patho-anatomy. Innovative open-source software, such as Horos™ [7] or OsiriX™, enable surgeons 3D visualization in any projection and the possibility to crop out unwanted areas, thereby enhancing their understanding of the patho-anatomy and of neighboring neurovascular structures. The multiplanar reconstruction of CT images offers a more precise planning for screw trajectories, as standard orthogonal CT slices are not aligned to the screw path [45]. This shrewdness further reduces the misplaced rate a fortiori when applied on intra-operative CT scan.

Additionally, it is important to underline that modern 3D reconstruction software can be used on laptops, enhancing the comfort and time spent for preoperative planning [76] (Fig. 2).

Fig. 2
figure 2

CT scan MPR reconstruction for planning screws trajectory using the open-source software Horos™

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In our experience, the blooming of these rousing resources allows a more precise, tailored, and targeted treatment relying on the most advanced classifications and indications for CVJ diseases, reducing both overtreatment and undertreatment [26, 27, 35, 40, 49, 73].

From this perspective, robot-assisted CVJ surgery arises as a natural evolution and thrilling innovation that could provide a platform to integrate intraoperative image acquisition, neuronavigation, artificial intelligence, and machine learning. The development of robot-assisted surgery has been met with interest in most surgical fields and in the last years also in cranial and spinal surgery. Nevertheless, currently, there are only few but interesting reports of robot-assisted CVJ surgery but the authors believe in the continued development of this technology [35, 40, 49, 73].

Implementation of navigation and robotic techniques is particularly helpful in performing challenging CVJ surgical procedures, when it comes to the accuracy of hardware insertion in proximity of vital neural and vascular structures. Nevertheless, it must be underlined that clinically acceptable accuracy of screw insertion, which means without clinical consequences to the patient, can be achieved in experienced hands with freehand fluoroscopy guidance [2, 5, 66].

Video-assisted surgical approaches to the CVJ

Nowadays, video-assisted procedures to the ventral skull base represent a commonly employed neurosurgical technique that has expanded the indications of endoscopic surgery. Moreover, the recent development of 3D endoscopes has allowed to overcome the 2-dimensional perception of the surgical field.

Endoscopic endonasal or transoral approaches make use of skull base anatomy to provide a direct corridor to the anterior clivus, C1 and C2, and have come to be accepted as alternatives to the more invasive microscopic transoral approaches in oncologic, traumatic, and degenerative pathologies of the CVJ, although they do carry certain disadvantages, namely, the technique’s learning curve and a restricted working channel. Moreover, transnasal approaches allow for reduction of local morbidity, as rhinolalia, dysphonia, dysphagia, and wound healing when compared to transoral approaches, and do not require a period of fasting in the postoperative period [13, 61].

In the last few years, this paradigm shift has also been clearly demonstrated in the management of CVJ pathologies [17, 24, 57, 74]. In 2022, Perrer et al. reported on their surgical series of 21 patients who underwent endoscopic endonasal odontoidectomy with favorable clinical courses at long-term follow-up, even in those cases with C1 arch preservation without posterior fixation [53], in line with the preliminary findings by Mazzatenta et al. [46].

The application of the video-assisted technologies to the anterior CVJ has given rise to multiple variations in the surgical technique: endoscopic endonasal approach, endoscopic transoral approach, robot-assisted endoscopic transoral approach, combined endoscopic transnasal and transoral approach, and endoscopic transcervical approach [69].

When assessing pathology in the CVJ in view of an endoscopic approach, the nasopalatine line—or Kassam line (also called K line)—can be drawn connecting the most inferior point of the nasal bone to the posterior edge of the hard palate and extending posteriorly in the midsagittal plane [10, 42] (Fig. 5). When the junction of the dens and the body of C2 is above this line, the endoscopic procedure can entirely be performed through the nose; otherwise, a combined endoscopic transnasal and transoral procedure should be preferred with visualization through the nose and the handling of instruments through the mouth [11].

Fig. 5
figure 5

The nasopalatine line, also known as Kassam line (K line), is the line that passes between the most inferior point of the nasal bone and the posterior edge of the hard palate extending posteriorly in the midsagittal plane. The purely endoscopic endonasal procedure for craniovertebral pathologies is suitable when the junction between the dens and the body of C2 is above this line; otherwise, a combined endoscopic endonasal and transoral procedure should be preferred

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The intraoperative position of the patient’s head is in slight flexion to allow a lower trajectory to the clivus and the CVJ. An extended approach is performed to expose the CVJ. After a wide posterior septostomy, the sphenoid sinus is opened, and its floor is removed with the Vidian nerve as the lateral limit. A nasopharyngeal flap is created starting just under the roof of the choana, in an inverted “U.” The upper half of the incision is carried through the nose, but in its lower extent, it is easier to raise this flap through the mouth. The lateral limits of the flap are medial to the Eustachian tube that represents an anatomical landmark for the parapharyngeal carotid artery. Finally, the attachments of the muscles are elevated off the clivus, anterior arch of C1, and dens (Fig. 6) [11].

Fig. 6
figure 6

Stepwise endoscopic approach to the foramen magnum and craniovertebral junction. a The alar ligaments (AR) are identified, as fibrous bands attacking to the posterolateral surface of the odontoid process and ascend obliquely and laterally to dock on the alar tubercles located on the medial side of the occipital condyles (OC). Odontoidectomy starts with drilling of the central core, of the odontoid process (OP). b, c After dens removal, the transverse ligament (blue star) can be seen extending between the transverse tubercles on the medial side of the C1 lateral masses (CC). The tectorial membrane (green arrow) spans from the transverse ligament (blue star) to the foramen magnum. d Final image of the extended endonasal approach to the clivus (CV). The right and left infratemporal fossae have been exposed, showing the path of the Eustachian tube (ET) and the branches of the mandibular nerve in depth (V3) (with permission of Pacca, P., Tardivo, V., Pecorari, G., Garbossa, D., Ducati, A., Zenga, F. (2019). The Endoscopic Endonasal Approach to Craniovertebral Junction Pathologies: Surgical Skills and Anatomical Study. In: Visocchi, M. (eds) New Trends in Craniovertebral Junction Surgery. Acta Neurochirurgica Supplement, vol 125. Springer, Cham. https://doi.org/10.1007/978-3-319-62515-7_5)

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The ongoing advancement in endoscopic skull base surgery has been transplanted to CVJ surgery to address anterior pathologies through a direct approach exploiting a close-up view of the relevant anatomy [16, 21, 53, 69]. In the past, microscopic transoral approaches proved to be effective treatments of oncologic, traumatic, and degenerative diseases of the CVJ. Nevertheless, this corridor was associated with complications and technical challenges. The introduction by the Pittsburgh group of the novel paradigm based on the endoscope and the endoscopic endonasal route allowed a straightforward access to the anterior CVJ for a 360° control of disease. Its use remains limited and technically demanding, mandating referral of such patients to specialized tertiary centers. We strongly believe that transnasal endoscopic approaches are nowadays a tremendous asset in CVJ surgery paraphernalia, having dramatically improved outcomes of patients requiring anterior decompression procedures at CVJ for tumoral and pseudo-tumoral diseases.

Increased safety at CVJ level has been obtained thanks to the implementation of endoscopic techniques for the abovementioned indications. Anterior open techniques to CVJ, e.g., transoral and transmaxillary, had been associated with an increased complication rate that is now extremely lowered by use of less invasive endoscopic guidance [17, 24, 53, 57].

Intraoperative neuromonitoring

In CVJ surgery, spinal cord injury occurs either primarily, through direct surgical maneuvers on the spinal cord or secondarily through indirect manipulation performed on the spine, such as traction or realignment [59].

In current practice, intraoperative monitoring is reliable to predict post-operative neurological deficits [30, 44]. In view of CVJ’s proximity to important neural structures, intraoperative neurophysiological monitoring (IONM) has found applications in CVJ surgery, with muscle motor-evoked potentials (mMEPs), corticospinal motor-evoked potentials (D-wave monitoring), and somatosensory evoked potentials (SSEPs) being its most frequently used modalities.

IONM might be of help in tumoral and traumatic pathologies at CVJ bolstering the safety during all the peri-operative maneuvers. In intradural tumors, despite the limitation in D-wave utilization, IONM might provide helpful information about preservation of the neural structures. Whereas, in traumatic cases, IONM might be used during positioning of intubated and unconscious patients [30, 44].

Certain CVJ surgeries may also require monitoring of lower cranial nerve function. Cranial nerves IX, X, XI, and XII can be monitored using free-running electromyography (EMG) and the triggered EMG map** technique. Recently, the mMEP technique has been used for the monitoring of the lower cranial nerves, where mMEPs are recorded by electrodes inserted into the muscles innervated by the lower motor cranial nerves. This technique has been shown to be more reliable than EMG [59].

In this context, we emphasize the ultimate role of intraoperative neuromonitoring in CVJ surgery reliability, which we use standardly use in our institution for all elective procedures, starting from the realignment maneuvers to patients repositioning into their bed. This allows for a timely monitoring of electrical conduction of neural elements during every phase of the surgery reducing the risk of unseen complications improving the safety throughout the whole procedure.

Conclusions

The CVJ was formerly considered a surgically challenging region with poor postoperative outcomes. This perception has gradually changed over past decades owing to advances in surgical technique and anatomical knowledge, progress in the diagnosis and treatment of CVJ pathology, and the development of novel technologies—such as navigation, robotics and video-assistance, and neuromonitoring—that facilitate surgical approaches to the CVJ and its instrumentation, while at the same time enhancing procedural safety. Nowadays, CVJ surgery is safer and widespread to an extent not imagined only 10–20 years ago. Research on biologics and biomaterials and the use 3D-printed technology to create tailored implants have shown favorable results on fusion rates and, from there, on long-term patient outcomes. The combined continued development in these fields likely augur further progress in the safety and efficiency of the surgical and peri-operative care of the CVJ. We look forward to the next years for the further development of biologics, biomaterials, artificial intelligence, and augmented reality bringing novel boosts in the safety of CVJ surgery.