Acta Neurochir (2014) 156:285–292 DOI 10.1007/s00701-013-1910-y
EXPERIMENTAL RESEARCH - NEUROSURGICAL TECHNIQUES
Anterior video-assisted approach to the craniovertebral junction: transnasal or transoral? A cadaver study Massimiliano Visocchi & Giuseppe La Rocca & Giuseppe Maria Della Pepa & Egidio Stigliano & Alessandro Costantini & Francesco Di Nardo & Giulio Maira
Received: 5 June 2013 / Accepted: 4 October 2013 / Published online: 26 October 2013 # Springer-Verlag Wien 2013
Abstract Background Endoscopy represents both an alternative and useful complement to the standard microsurgical approach to the anterior craniovertebral junction (CVJ). Nevertheless, few studies provide an experimental comparison between transnasal and transoral endoscopic control on CVJ. We compared the surgical exposition angle and the working channel volume of both the transnasal and transoral approaches in the cadaver. Methods Eleven fresh non-perfused cadavers were studied. Transnasal and transoral linear and angled exposure of the CVJ were evaluated by means of X-ray and CT scan both in sagittal and lateral planes. Results The transoral endoscopic surgical exposition was wider compared with the transnasal in anterior and lateral projections:(1)in the sagittal plane, both in vertical exposition (transnasal inferior to transoral from 5.89 % to 76.48 %, average 35.89 %) and in vertical surgical angle (from 22 % to 77.42 %, average 56.53 %); (2)in the coronal plane, both in coronal exposition (transnasal inferior to transoral from 50.77 % to 83.88 %, average 70.34 %) and in coronal surgical angle (from 65.58 % to 86.71 %, average 76.70 %). The M. Visocchi : G. La Rocca : G. M. Della Pepa (*) : G. Maira Institute of Neurosurgery, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy e-mail: [email protected] E. Stigliano Institute of Pathology, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy A. Costantini Institute of Radiology, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy F. Di Nardo Institute of Hygiene, Epidemiology and Biostatistics, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy
sagittal surgical domain was found to spanning from the inferior third of the clivus to C3 with the transoral and from the middle third of the clivus to the nasopalatal line (NPL) with the transnasal approach. The overlapping surgical domain area was found to be the inferior third of the clivus. Conclusions The endoscope assisted transoral approach allows a better surgical control of the CVJ. It provides a better CVJ exposure, in sagittal and transverse planes, providing a larger working channel and an easier manoeuvrability. The transnasal approach is limited in caudal direction down to the NPL, otherwise the transoral approach is limited in the rostral direction with a maximum to the foramen magnum in normal specimen. In every individual case, pros and cons of the appropriate approach have to be taken into account as well as the choice of a combined transnasal and transoral approaches strategy. Keywords Craniovertebral junction . Transoral approach . Transnasal approach . Endoscopy . Cadaver lab
Introduction In 1962, Fang and Ong [5] published the first series of patients who underwent transoral decompression for irreducible atlantoaxial abnormalities. The high rate of morbidity and mortality discouraged the use of the transoral approach as a tool for decompression of anterior craniovertebral junction (CVJ) abnormalities. The transoral approach to the posterior pharyngeal wall has been used for years to drain retropharyngeal abscesses, but only in the 1940s was it first proposed for the treatment of spinal abnormalities [5, 14]. Popularised by Crockard [3], the microsurgical ventral approach to the CVJ has been widely described for decompression of irreducible extradural pathology [16, 18]. The shortest and most physiological route to the ventral aspect
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of the CVJ is represented by an anterior approach through the pharynx. A number of anterior approaches have been described to allow exposure to the midline and lateral aspects of both the cranial base and upper cervical spine [11]. The transoral-transpharyngeal approach, a technique that is well known to many spine surgeons, provides surgical access to the anterior clivus, C1 and C2. The use of the operating microscope, high-speed drills, self-retaining mouth retractors, flexible oral endotracheal tubes, intra-operative fluoroscopy, neuronavigation and electrophysiological monitoring has made this procedure much more safer [11, 15–17, 19]. In order to overcome the need of soft palate splitting or more complex jaw-splitting approaches (i.e. transoral approach with transmaxillary extention), endoscopic assisted procedures for CVJ decompression have been developed, starting from the experience with the use of the endoscope for the transsphenoidal pituitary surgery since 2002 up to the first clinical application of Kassam et al. in 2005 [8–10]. So far experimental cadaveric studies have been performed on the feasibility of the endoscopic transnasal approach as well as on the comparison between microsurgical and endoscopic transoral approach without any neuroradiological assessment [1, 2, 6, 8, 11]. Only one paper examined and compared both the straight and angled telescopes showing the upper and lower limits of the transnasal and transoral approaches to the CVJ as defined with the straight stealth probe but without a contextual “real time” neuroadiological evaluation of both transnasal and transoral surgical domains at open mouth with oral distractor [12]. In the present study we compared the surgical exposition angle and the working channel volume of both transnasal and transoral approaches in the cadaver by means of a comparative neuroradiological “real time” study. To our knowledge such a comparison have never been performed in order to prove the possible supremacy of transnasal or transoral approaches in controlling CVJ anatomical normal region.
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tubercle of C1 was identified with the finger in all the cadavers and the position of the distractor was chosen according to the fluoroscopic assessment (MPX+ portable X-ray unit; Philips Healthcare, Best, The Netherlands). By the use of thin stainless probes (30 cm length) inserted trough the nostrils (choanae) and the oral cavity, the transnasal (through both nostrils) and the transoral (through the oral cavity as exposed by the Crockard distractor), maximum linear and angled exposure of CVJ were evaluated by means of X-ray and CT scan (GE LightSpeed VCT 64 Slice; General Electric, Milwauchee, WI, USA) both in sagittal and lateral study (Figs. 1, 2 and 3). All the patients except two (nine subjects, 81.8 % of the sample) underwent CT imaging and Xray in lateral and anterior projections; two subjects (11.2 %) were studied only with X-ray in lateral and anterior projections. The values of the linear (cm) and the angular (°) expositions of the transoral and the transnasal approaches were evaluated for each subject by the lateral and the anterior X-rays (Tables 1 and 2). Percentage differences (%) of the transoral to the transnasal approach were calculated for each subject as follows: 1. Transnasal/transoral linear exposition (cm) × 100, both for the vertical and the lateral study 2. Transnasal/transoral exposition angle (°) × 100, both for the vertical and the lateral study These results are reported in Tables 1 and 2. The surgical domain of both approaches on the sagittal plane was evaluated by considering the nasopalatal line (NPL) as the reference point in order to know the actual anatomical areas covered by both approaches and how they overlap [4]. No platibasia or impression basilaris were identified radiologically, nor was jaw opening impairment found in any of the cadavers. Collected data were statistically analysed.
Methods Statistical analysis After obtaining the Ethical Committee Approval of the experimental protocol by the Catholic University of Rome, Italy (protocol number P663/CE/2010 approved on July 28th, 2010; subsequent amendment number P437/CE 2012 approved on May 2nd, 2012) 11 fresh non-perfused cadavers—six female (54.5 %) and five male (45.6 %)— median age 75 years (IQ range 35; minimum 42, maximum 98), were studied in the sectorial room of the Institute of Pathology of our university. In supine position with the head lightly extended (about 25°) the Crockard transoral distractor (Crockard Transoral Instrument Set; Codman and Shurtleff, Raynham, MA, USA) was put in the oral cavity to expose the CVJ. The
A descriptive analysis of the sample was carried out by means of median, interquartile range (IQR) and range for continuous variables, and absolute and relative frequencies for qualitative ones. In order to find statistically significant differences between the two surgical approaches, we performed a Wilcoxon signed rank test. We chose to use a non-parametric test because data were not normally distributed as demonstrated by ShapiroWilk test [13]. The analysis was performed using SPSS software version 12.0 for Windows and statistical significance level was set at p =0.05.
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Fig. 1 Cadaver lateral view of transnasal and transoral probes with the oral distractor: left lateral view; right AP view
Results X-ray and CT scan measurements of CVJ fitted in all the subjects. On the sagittal plane, statistically significant differences of C0-C1-C2 coverage were observed between the two surgical techniques in terms of both explored vertical distances (p = 0.003) and vertical exposition angle (p =0.003), with the transnasal approach allowing less extensive exploration. The sagittal surgical domain was found to span from the inferior third of the clivus (1 cm above the NPL) to C3 with the transoral approach and from the middle third of the clivus (more than 2 cm above the NPL) to the NPL with the transnasal approach. The overlapping surgical domain area was found to be the inferior third of the clivus. On the frontal plane there were statistically significant differences both in the explored horizontal distances (p = 0.008) and in the horizontal exposition angle (p =0.008), with the transnasal technique allowing less extensive exploration (Tables 1, 2 and 3; Figs. 4 and 5). A better exposure of the CVJ (C0-C1-C2) was obtained by using the transoral approach rather than the transnasal approach, both in anterior and lateral projection. In more detail, from a gross numerical point of view, the transnasal endoscopic surgical exposition was inferior compared with the transoral for the linear and angular surgical domain: 1. In the sagittal plane, from a minimum of 5.89 % to a maximum of 76.48 % (average 35.89 %) as vertical surgical exposition and from a minimum of 22 % to a Fig. 2 CT scan sagittal reconstruction of vertical transnasal (left) and transoral (right) control of CVJ
maximum of 77.42 % as vertical surgical route angle (average 56.53 %) with less surgical control caudally to the NPL 2. In the coronal plane, from a minimum of 50.77 % to a maximum of 83.88 % (average 70.34 %) as coronal surgical exposition and from a minimum of 65.58 % to a maximum of 86.71 % as coronal surgical route angle (average 76.70 %) with less surgical control lateral to the oropharinx
Discussion The transnasal endoscopic approach The increased diffusion in the use of the endoscope for transsphenoidal pituitary surgery led some studies to explore the possibility of applying the endoscopic endonasal approach in the surgical treatment of skull base lesions other than pituitary tumours. In recent years some papers have reported anatomical studies and surgical experience in the endoscopic endonasal approach to different areas of the midline skull base, from the olfactory groove to the CVJ [8]. In 2002, Alfieri et al. [1] was the first to perform a cadaveric study on totally transnasal endoscopic odontoidectomy through a one- or twonostril route, by following the endonasal paraseptal technique of Jho and Ha [7]. The surgical landmarks leading to the CVJ were the inferior margin of the middle turbinate, nasopharynx
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Fig. 3 CT scan frontal reconstruction of left nostril transnasal (left), right nostril transnasal (centre) and transoral (right) control of CVJ
and the Eustachian tubes. The nasopharynx was readily identified following the inferior margin of the middle turbinate. The line drawn between the Eustachian tubes indicated the juncture between the clivus and atlas. The authors concluded that “contrary to a conventional transoral approach, this endoscopic endonasal approach provides unlimited access to the midline clivus and a potential of carrying out surgical decompression at the ventral craniocervical junction without adding C1-2 instability” [1]. Three years later, Cavallo et al. [2] confirmed such an observation on cadaveric study. After the intuition of Alfieri and co-workers, in 2005 Kassam et al. [8] operated the first case through a fully transnasal endoscopic resection of the odontoid [8]. In his report, Kassam and co-workers concluded: “The transoral approach remains the ‘gold standard’”, but in contrast with this “the defect created by transnasal approach is above the level of soft palate and should
not be exposed to the same degree of bacterial contamination”. Further anatomical studies performed by Messina et al. [9] 1 year later concluded that similar to the transoral approach, the endoscopic endonasal provides a direct route to the surgical target, but it seems related to less morbidity. Nevertheless, as matter of fact things are less simple. In 2009, de Almeida et al. [4] published the concept of the NPL which is the line created by connecting the most inferior point on the nasal bone to the most posterior point on the hard palate in the midsagittal plane. Intersection of this line with the vertebral column is measured relative to the inferior aspect of the body of C2 along its posterior surface. The NPL is a reliable predictor of the maximal extent of inferior dissection, and odontoid surgery can reliably be performed according to the preoperative radiological study of the possible anatomical limitations of the endonasal approach. This approach is
Table 1 Lateral X-ray: vertical exposition and surgical angles. Comparison between transnasal and transoral approaches Age (years)
90 56 80 79 98 55 94 51 42 75 69
Sex
F M F F F M F M M M F
Transoral approach: vertical exposition (cm)/surgical angle
6.176/45° 3.552/46° 5.795/60° 6.5/62° 6.75/63° 5.65/58° 4.428/50° 5.714/51° 6.075/50° 6.31/69° 4.25/45°
Transnasal approach: vertical exposition (cm)/surgical angle
4.588/22° 2.289/14° 5.454/30° 2.214/14° 5.4/32° 4.875/24° 2.142/14° 4.428/28° 4.65/39° 2.91/29° 1/14°
Vertical exposition (cm)
Surgical angle
Transnasal / transoral (%)
Percent superiority of transoral to transnasal
Transnasal / transoral (%)
Percent superiority of transoral to transnasal
74.28 % 64.44 % 94.11 % 34.06 % 80 % 86.25 % 48.37 % 77.49 % 76.54 % 46.11 % 23.52 %
25.72 % 35.56 % 5.89 % 65.94 % 20 % 13.75 % 51.63 % 22.51 % 23.46 % 53.89 % 76.48 %
48.88 % 30.43 % 50 % 22.58 % 50.79 % 41.37 % 28 % 54.90 % 78 % 42.02 % 31.11 %
51.12 69.57 50 % 77.42 49.21 58.63 72 % 45.10 22 % 57.98 68.89
% % % % % % % %
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Table 2 Anterior X-ray: vertical exposition and surgical angles. Comparison between transnasal and transoral approaches Age (years)
Sex
Transoral approach: vertical exposition (cm)/surgical angle
Transnasal approach: vertical exposition (cm)/surgical angle
Vertical exposition (cm)
Surgical angle
Transnasal / transoral(%)
Percent superiority of transoral to transnasal
Transnasal / transoral(%)
Percent superiority of transoral to transnasal
90
F
ND
ND
ND
ND
ND
ND
56 80 79 98 55 94 51 42 75 69
M F F F M F M M M F
ND 4.930/124° 8.266/95° 6.866/138° 4.62/146° 6/156° 6.4/152° 6.533/158° 4.31/122° 4.55/140°
ND 1.533/26° 1.333/22° 1.544/40° 1.98/34° 1.2/22° 1.22/36° 1.133/21° 2.1/42° 2.24/39°
ND 31.09 16.12 22.48 42.85 20 % 19.06 17.34 48.72 49.23
ND 68.91 83.88 77.52 57.15 80 % 80.94 82.66 51.28 50.77
ND 20.96 23.15 28.98 23.28 14.10 23.68 13.29 34.42 27.85
ND 79.04 76.85 71.02 76.72 85.90 76.32 86.71 65.58 72.15
% % % % % % % %
% % % % % % % %
% % % % % % % % %
% % % % % % % % %
ND not determined
recommended in selected cases as a valid alternative to the transoral microscopic approach for the resection of the odontoid process of C2 and should be performed only by surgeons very skilled in endoscopic endonasal surgery and in endoscopic cadaver dissections [15]. The transoral endoscopic approach The 30-degree endoscope has been proposed for the transoral approach to avoid full soft-palate splitting, hard-palate splitting or extended maxillo/mandibulotomy [7, 9]. Using the endoscope, the operator is able to look in all directions by rotating the instrument. Because the light source is at the level of the abnormality, superior illumination can be obtained. With the aid of an endoscope, abnormalities as high as the mid-clivus can be visualised without extensive soft- or hard-palate manipulation [11, 16, 17].
The last high profile cadaveric study recently available in the literature is the one of Pillai et al. [11], which quantifies the surgical volume gained by this approach: the surgical area exposed over the posterior pharyngeal wall is significantly improved using the endoscope (606.5–127.4 mm3) compared with the operating microscope (425.7–100.8 mm3), without any compromise of surgical freedom (p = 0.05). The extent of the clivus exposed with the endoscope (9.5±0.7 mm) without splitting the soft palate is significantly improved compared with that associated with microscopic approach (2.0±0.4 mm) (p = 0.05) [11].
The present cadaveric study Our study on the cadaver is the first experience dealing with contextual neuroradiological “real time” examination and
Table 3 Transoral approach versus transnasal approach. Vertical and horizontal explorable distances and exposition angles Variable
Median (IQ range)
Minimum-maximum
SD
pa
Transoral approachb (vertical exposition, cm) Transnasal approach (vertical exposition, cm) Transoral approachb (vert. exposition angle) Transnasal approach (vert. exposition angle) Transoral approachc (horizontal exposition, cm) Transnasal approach (horizontal exposition, cm) Transoral approachc (horiz. exposition angle) Transnasal approach (horiz. exposition angle)
5.719 (1.365) 4.428 (2.960) 58 (13) 28 (17) 6.000 (2.115) 1.533 (0.830) 140 (31) 34 (18)
4.250–6.750 1.000–5.454 45–69 14–39 4.310–8.266 1.133–2.240 95–158 21–42
1.03 1.55 8.28 8.76 1.32 0.4 13.69 8.34
0.003
SD standard deviation a
Wilcoxon signed rank test
b
11 subjects
c
9 subjects
0.003 0.008 0.008
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Fig. 4 Median explorable distances (cm). Transoral vs transnasal approach
comparison of both transnasal and transoral CVJ surgical domains in the same subject. The impact of CVJ pathology is not addressed by this study; of course, cranial settling, CVJ kyphotic deformity and other changes will alter the relative utility of the two approaches. In fact, it must be pointed out that we studied only “normal” cadavers and, since the most common diseases found at this area are os odontoideum and basal invagination, in both circumstances, the tip of the dens is not easy to resect via the mouth. Moreover, different areas of exposure are not all of equal value for each operative goal and simple area or angle measurements cannot address this. Since the angles and distances are highly abstract for a surgeon and to know which Fig. 5 Median exposition angle (degrees). Transoral vs transnasal approach
anatomical structure can be reached with the two approaches, and which structures have to be destructed to reach the final target is mandatory, we used the NPL as ideal reference point to compare both surgical strategies. Nevertheless our study allows us to state that the transnasal approach, as it has already been widely discussed, is a viable strategy to reach the CVJ, but has limited angular (nostrils, choanae) and linear (NPL) surgical exposure, which in our view makes it suitable only for certain types of diseases and prevents its systematic applicability in other conditions, such as lateral tumours and pathologies caudal to C2. Although an obvious advantage of this approach is that there is no need to cut the soft palate, which minimises the potential postoperative morbidity like swallowing disturbances and
Acta Neurochir (2014) 156:285–292
hyper-nasal speech, which are really limiting to quality of life (lack palatine veil); the transoral approach provides a better exposure of the CVJ, both on the sagittal plane and on the transverse plane, providing a larger working channel and allowing an easier manoeuvrability of surgical instruments such as the endoscope [6]. With this tool, the advantage of the soft palate sparing might make the transnasal endoscopic approach less competitive compared with the transoral endoscopic assisted one. Finally, the potential for combining the two approaches to accomplish a particular surgical goal must be considered also a potential option. In our experience, we have used the endoscopic transoral route mainly in conjunction with the endoscopic transnasal approach to pathologies of the lower clivus such as chordomas. This shows that the two approaches are not competitive and can easily be used together to treat lesions that extend beyond the exposure limits of one or the other approach alone.
Conclusions Endoscopic endonasal and transoral approaches developed recently as promising alternatives to the classic microsurgical transoral approach to the CVJ (Table 4). From the pure anatomic point of view, our study seems to suggest that in normal conditions the transnasal approach to the CVJ is an oblique approach, which allows only the piecemeal removal of CVJ pathology and is not recommended for large tumours and low, and far laterally sited CVJ pathologies. The transnasal approach is limited in the caudal direction down to the NPL; otherwise the transoral approach is limited in the rostral direction with a maximum to the foramen magnum in a normal specimen. In every individual case, pros and cons of the appropriate approach have to be taken into account as well as the choice of a combined transnasal and transoral approach strategy.
Table 4 Transnasal and transoral: pros and cons of each approach Transnasal approach Pros: Partial isolation of the oral cavity, no needs of tracheostomy and reduced need of feeding tube. Cons: Oblique approach, only piecemeal removal of CVJ pathology is allowed, not recommended for large tumours and low sited CVJ pathologies. Transoral approach Pros: Direct approach, radical removal of huge tumours, good visualisation and comfortable mobilisation of surgical tools. Cons: Possible need of tracheostomy, need of feeding tube, difficult management of very high invagination conditions with platibasia.
291 Conflicts of interest None. Disclosure The authors declare no interest to disclose, they have any personal or institutional financial interest in drugs, materials or devices described in this submission and that they did not receive any specific funding.
References 1. Alfieri A, Jho HD, Tschabitscher M (2002) Endoscopic endonasal approach to the ventral cranio-cervical junction: anatomical study. Acta Neurochir (Wien) 144:219–225, discussion 225 2. Cavallo LM, Messina A, Cappabianca P, Esposito F, de Divitiis E, Gardner P, Tschabitscher M (2005) Endoscopic endonasal surgery of the midline skull base: anatomical study and clinical considerations. Neurosurg Focus 19:E2 3. Crockard HA (1991) Ventral approaches to the upper cervical spine. Orthopade 20:140–146 4. de Almeida JR, Zanation AM, Snyderman CH, Carrau RL, Prevedello DM, Gardner PA, Kassam AB (2009) Defining the nasopalatine line: the limit for endonasal surgery of the spine. Laryngoscope 119:239–244 5. Fang HSY, Ong GB (1962) Direct anterior approach to the upper cervical spine. J Bone Joint Surg Am 44A:1588–1604, 1962, J Bone Joint Surg Am 44A:1588–1604 6. Frempong-Boadu AK, Faunce WA, Fessler RG (2002) Endoscopically assisted transoral-transpharyngeal approach to the craniovertebral junction. Neurosurgery 51:S60–S66 7. Jho HD, Ha HG (2004) Endoscopic endonasal skull base surgery: part 3—The clivus and posterior fossa. Minim Invasive Neurosurg 47:16–23 8. Kassam AB, Snyderman C, Gardner P, Carrau R, Spiro R (2005) The expanded endonasal approach: a fully endoscopic transnasal approach and resection of the odontoid process: technical case report. Neurosurgery 57:E213, discussion E213 9. Messina A, Bruno MC, Decq P, Coste A, Cavallo LM, de Divittis E, Cappabianca P, Tschabitscher M (2007) Pure endoscopic endonasal odontoidectomy: anatomical study. Neurosurg Rev 30:189–194, discussion 194 10. Oya S, Tsutsumi K, Shigeno T, Takahashi H (2004) Posterolateral odontoidectomy for irreducible atlantoaxial dislocation: a technical case report. Spine J 4:591–594 11. Pillai P, Baig MN, Karas CS, Ammirati M (2009) Endoscopic imageguided transoral approach to the craniovertebral junction: an anatomic study comparing surgical exposure and surgical freedom obtained with the endoscope and the operating microscope. Neurosurgery 64:437–442, discussion 442–434 12. Seker A, Inoue K, Osawa S, Akakin A, Kilic T, Rhoton AL Jr (2010) Comparison of endoscopic transnasal and transoral approaches to the craniovertebral junction. World Neurosurg 74:583–602 13. Shapiro S, Wilk MB, Chen HJA (1968) Comparative study of various tests for normality. J Am Stat Assoc 63:1343–1372 14. Symonds CPMS (1937) Compression of the spinal cord in the neighborhood of the foramen magnum with a note on the surgical approach by Julian Taylor. Brain 60:52–84 15. Visocchi M (2011) Advances in videoassisted anterior surgical approach to the craniovertebral junction. Adv Tech Stand Neurosurg 37:97–110 16. Visocchi M, Della Pepa GM, Doglietto F, Esposito G, La Rocca G, Massimi L (2011) Video-assisted microsurgical transoral approach to the craniovertebral junction: personal experience in childhood. Childs Nerv Syst 27:825–831
292 17. Visocchi M, Doglietto F, Della Pepa GM, Esposito G, La Rocca G, Di Rocco C, Maira G, Fernandez E (2011) Endoscope-assisted microsurgical transoral approach to the anterior craniovertebral junction compressive pathologies. Eur Spine J 20:1518–1525 18. Visocchi M, Pietrini D, Tufo T, Fernandez E, Di Rocco C (2009) Preoperative irreducible C1-C2 dislocations: intra-operative reduction
Acta Neurochir (2014) 156:285–292 and posterior fixation. The “always posterior strategy”. Acta Neurochir (Wien) 151:551–559 19. Vougioukas VI, Hubbe U, Schipper J, Spetzger U (2003) Navigated transoral approach to the cranial base and the craniocervical junction: technical note. Neurosurgery 52:247–250, discussion 251
EXPERIMENTAL RESEARCH - NEUROSURGICAL TECHNIQUES
Anterior video-assisted approach to the craniovertebral junction: transnasal or transoral? A cadaver study Massimiliano Visocchi & Giuseppe La Rocca & Giuseppe Maria Della Pepa & Egidio Stigliano & Alessandro Costantini & Francesco Di Nardo & Giulio Maira
Received: 5 June 2013 / Accepted: 4 October 2013 / Published online: 26 October 2013 # Springer-Verlag Wien 2013
Abstract Background Endoscopy represents both an alternative and useful complement to the standard microsurgical approach to the anterior craniovertebral junction (CVJ). Nevertheless, few studies provide an experimental comparison between transnasal and transoral endoscopic control on CVJ. We compared the surgical exposition angle and the working channel volume of both the transnasal and transoral approaches in the cadaver. Methods Eleven fresh non-perfused cadavers were studied. Transnasal and transoral linear and angled exposure of the CVJ were evaluated by means of X-ray and CT scan both in sagittal and lateral planes. Results The transoral endoscopic surgical exposition was wider compared with the transnasal in anterior and lateral projections:(1)in the sagittal plane, both in vertical exposition (transnasal inferior to transoral from 5.89 % to 76.48 %, average 35.89 %) and in vertical surgical angle (from 22 % to 77.42 %, average 56.53 %); (2)in the coronal plane, both in coronal exposition (transnasal inferior to transoral from 50.77 % to 83.88 %, average 70.34 %) and in coronal surgical angle (from 65.58 % to 86.71 %, average 76.70 %). The M. Visocchi : G. La Rocca : G. M. Della Pepa (*) : G. Maira Institute of Neurosurgery, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy e-mail: [email protected] E. Stigliano Institute of Pathology, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy A. Costantini Institute of Radiology, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy F. Di Nardo Institute of Hygiene, Epidemiology and Biostatistics, Catholic University of Rome, Largo Gemelli, 8, 00168 Rome, Italy
sagittal surgical domain was found to spanning from the inferior third of the clivus to C3 with the transoral and from the middle third of the clivus to the nasopalatal line (NPL) with the transnasal approach. The overlapping surgical domain area was found to be the inferior third of the clivus. Conclusions The endoscope assisted transoral approach allows a better surgical control of the CVJ. It provides a better CVJ exposure, in sagittal and transverse planes, providing a larger working channel and an easier manoeuvrability. The transnasal approach is limited in caudal direction down to the NPL, otherwise the transoral approach is limited in the rostral direction with a maximum to the foramen magnum in normal specimen. In every individual case, pros and cons of the appropriate approach have to be taken into account as well as the choice of a combined transnasal and transoral approaches strategy. Keywords Craniovertebral junction . Transoral approach . Transnasal approach . Endoscopy . Cadaver lab
Introduction In 1962, Fang and Ong [5] published the first series of patients who underwent transoral decompression for irreducible atlantoaxial abnormalities. The high rate of morbidity and mortality discouraged the use of the transoral approach as a tool for decompression of anterior craniovertebral junction (CVJ) abnormalities. The transoral approach to the posterior pharyngeal wall has been used for years to drain retropharyngeal abscesses, but only in the 1940s was it first proposed for the treatment of spinal abnormalities [5, 14]. Popularised by Crockard [3], the microsurgical ventral approach to the CVJ has been widely described for decompression of irreducible extradural pathology [16, 18]. The shortest and most physiological route to the ventral aspect
286
of the CVJ is represented by an anterior approach through the pharynx. A number of anterior approaches have been described to allow exposure to the midline and lateral aspects of both the cranial base and upper cervical spine [11]. The transoral-transpharyngeal approach, a technique that is well known to many spine surgeons, provides surgical access to the anterior clivus, C1 and C2. The use of the operating microscope, high-speed drills, self-retaining mouth retractors, flexible oral endotracheal tubes, intra-operative fluoroscopy, neuronavigation and electrophysiological monitoring has made this procedure much more safer [11, 15–17, 19]. In order to overcome the need of soft palate splitting or more complex jaw-splitting approaches (i.e. transoral approach with transmaxillary extention), endoscopic assisted procedures for CVJ decompression have been developed, starting from the experience with the use of the endoscope for the transsphenoidal pituitary surgery since 2002 up to the first clinical application of Kassam et al. in 2005 [8–10]. So far experimental cadaveric studies have been performed on the feasibility of the endoscopic transnasal approach as well as on the comparison between microsurgical and endoscopic transoral approach without any neuroradiological assessment [1, 2, 6, 8, 11]. Only one paper examined and compared both the straight and angled telescopes showing the upper and lower limits of the transnasal and transoral approaches to the CVJ as defined with the straight stealth probe but without a contextual “real time” neuroadiological evaluation of both transnasal and transoral surgical domains at open mouth with oral distractor [12]. In the present study we compared the surgical exposition angle and the working channel volume of both transnasal and transoral approaches in the cadaver by means of a comparative neuroradiological “real time” study. To our knowledge such a comparison have never been performed in order to prove the possible supremacy of transnasal or transoral approaches in controlling CVJ anatomical normal region.
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tubercle of C1 was identified with the finger in all the cadavers and the position of the distractor was chosen according to the fluoroscopic assessment (MPX+ portable X-ray unit; Philips Healthcare, Best, The Netherlands). By the use of thin stainless probes (30 cm length) inserted trough the nostrils (choanae) and the oral cavity, the transnasal (through both nostrils) and the transoral (through the oral cavity as exposed by the Crockard distractor), maximum linear and angled exposure of CVJ were evaluated by means of X-ray and CT scan (GE LightSpeed VCT 64 Slice; General Electric, Milwauchee, WI, USA) both in sagittal and lateral study (Figs. 1, 2 and 3). All the patients except two (nine subjects, 81.8 % of the sample) underwent CT imaging and Xray in lateral and anterior projections; two subjects (11.2 %) were studied only with X-ray in lateral and anterior projections. The values of the linear (cm) and the angular (°) expositions of the transoral and the transnasal approaches were evaluated for each subject by the lateral and the anterior X-rays (Tables 1 and 2). Percentage differences (%) of the transoral to the transnasal approach were calculated for each subject as follows: 1. Transnasal/transoral linear exposition (cm) × 100, both for the vertical and the lateral study 2. Transnasal/transoral exposition angle (°) × 100, both for the vertical and the lateral study These results are reported in Tables 1 and 2. The surgical domain of both approaches on the sagittal plane was evaluated by considering the nasopalatal line (NPL) as the reference point in order to know the actual anatomical areas covered by both approaches and how they overlap [4]. No platibasia or impression basilaris were identified radiologically, nor was jaw opening impairment found in any of the cadavers. Collected data were statistically analysed.
Methods Statistical analysis After obtaining the Ethical Committee Approval of the experimental protocol by the Catholic University of Rome, Italy (protocol number P663/CE/2010 approved on July 28th, 2010; subsequent amendment number P437/CE 2012 approved on May 2nd, 2012) 11 fresh non-perfused cadavers—six female (54.5 %) and five male (45.6 %)— median age 75 years (IQ range 35; minimum 42, maximum 98), were studied in the sectorial room of the Institute of Pathology of our university. In supine position with the head lightly extended (about 25°) the Crockard transoral distractor (Crockard Transoral Instrument Set; Codman and Shurtleff, Raynham, MA, USA) was put in the oral cavity to expose the CVJ. The
A descriptive analysis of the sample was carried out by means of median, interquartile range (IQR) and range for continuous variables, and absolute and relative frequencies for qualitative ones. In order to find statistically significant differences between the two surgical approaches, we performed a Wilcoxon signed rank test. We chose to use a non-parametric test because data were not normally distributed as demonstrated by ShapiroWilk test [13]. The analysis was performed using SPSS software version 12.0 for Windows and statistical significance level was set at p =0.05.
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287
Fig. 1 Cadaver lateral view of transnasal and transoral probes with the oral distractor: left lateral view; right AP view
Results X-ray and CT scan measurements of CVJ fitted in all the subjects. On the sagittal plane, statistically significant differences of C0-C1-C2 coverage were observed between the two surgical techniques in terms of both explored vertical distances (p = 0.003) and vertical exposition angle (p =0.003), with the transnasal approach allowing less extensive exploration. The sagittal surgical domain was found to span from the inferior third of the clivus (1 cm above the NPL) to C3 with the transoral approach and from the middle third of the clivus (more than 2 cm above the NPL) to the NPL with the transnasal approach. The overlapping surgical domain area was found to be the inferior third of the clivus. On the frontal plane there were statistically significant differences both in the explored horizontal distances (p = 0.008) and in the horizontal exposition angle (p =0.008), with the transnasal technique allowing less extensive exploration (Tables 1, 2 and 3; Figs. 4 and 5). A better exposure of the CVJ (C0-C1-C2) was obtained by using the transoral approach rather than the transnasal approach, both in anterior and lateral projection. In more detail, from a gross numerical point of view, the transnasal endoscopic surgical exposition was inferior compared with the transoral for the linear and angular surgical domain: 1. In the sagittal plane, from a minimum of 5.89 % to a maximum of 76.48 % (average 35.89 %) as vertical surgical exposition and from a minimum of 22 % to a Fig. 2 CT scan sagittal reconstruction of vertical transnasal (left) and transoral (right) control of CVJ
maximum of 77.42 % as vertical surgical route angle (average 56.53 %) with less surgical control caudally to the NPL 2. In the coronal plane, from a minimum of 50.77 % to a maximum of 83.88 % (average 70.34 %) as coronal surgical exposition and from a minimum of 65.58 % to a maximum of 86.71 % as coronal surgical route angle (average 76.70 %) with less surgical control lateral to the oropharinx
Discussion The transnasal endoscopic approach The increased diffusion in the use of the endoscope for transsphenoidal pituitary surgery led some studies to explore the possibility of applying the endoscopic endonasal approach in the surgical treatment of skull base lesions other than pituitary tumours. In recent years some papers have reported anatomical studies and surgical experience in the endoscopic endonasal approach to different areas of the midline skull base, from the olfactory groove to the CVJ [8]. In 2002, Alfieri et al. [1] was the first to perform a cadaveric study on totally transnasal endoscopic odontoidectomy through a one- or twonostril route, by following the endonasal paraseptal technique of Jho and Ha [7]. The surgical landmarks leading to the CVJ were the inferior margin of the middle turbinate, nasopharynx
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Fig. 3 CT scan frontal reconstruction of left nostril transnasal (left), right nostril transnasal (centre) and transoral (right) control of CVJ
and the Eustachian tubes. The nasopharynx was readily identified following the inferior margin of the middle turbinate. The line drawn between the Eustachian tubes indicated the juncture between the clivus and atlas. The authors concluded that “contrary to a conventional transoral approach, this endoscopic endonasal approach provides unlimited access to the midline clivus and a potential of carrying out surgical decompression at the ventral craniocervical junction without adding C1-2 instability” [1]. Three years later, Cavallo et al. [2] confirmed such an observation on cadaveric study. After the intuition of Alfieri and co-workers, in 2005 Kassam et al. [8] operated the first case through a fully transnasal endoscopic resection of the odontoid [8]. In his report, Kassam and co-workers concluded: “The transoral approach remains the ‘gold standard’”, but in contrast with this “the defect created by transnasal approach is above the level of soft palate and should
not be exposed to the same degree of bacterial contamination”. Further anatomical studies performed by Messina et al. [9] 1 year later concluded that similar to the transoral approach, the endoscopic endonasal provides a direct route to the surgical target, but it seems related to less morbidity. Nevertheless, as matter of fact things are less simple. In 2009, de Almeida et al. [4] published the concept of the NPL which is the line created by connecting the most inferior point on the nasal bone to the most posterior point on the hard palate in the midsagittal plane. Intersection of this line with the vertebral column is measured relative to the inferior aspect of the body of C2 along its posterior surface. The NPL is a reliable predictor of the maximal extent of inferior dissection, and odontoid surgery can reliably be performed according to the preoperative radiological study of the possible anatomical limitations of the endonasal approach. This approach is
Table 1 Lateral X-ray: vertical exposition and surgical angles. Comparison between transnasal and transoral approaches Age (years)
90 56 80 79 98 55 94 51 42 75 69
Sex
F M F F F M F M M M F
Transoral approach: vertical exposition (cm)/surgical angle
6.176/45° 3.552/46° 5.795/60° 6.5/62° 6.75/63° 5.65/58° 4.428/50° 5.714/51° 6.075/50° 6.31/69° 4.25/45°
Transnasal approach: vertical exposition (cm)/surgical angle
4.588/22° 2.289/14° 5.454/30° 2.214/14° 5.4/32° 4.875/24° 2.142/14° 4.428/28° 4.65/39° 2.91/29° 1/14°
Vertical exposition (cm)
Surgical angle
Transnasal / transoral (%)
Percent superiority of transoral to transnasal
Transnasal / transoral (%)
Percent superiority of transoral to transnasal
74.28 % 64.44 % 94.11 % 34.06 % 80 % 86.25 % 48.37 % 77.49 % 76.54 % 46.11 % 23.52 %
25.72 % 35.56 % 5.89 % 65.94 % 20 % 13.75 % 51.63 % 22.51 % 23.46 % 53.89 % 76.48 %
48.88 % 30.43 % 50 % 22.58 % 50.79 % 41.37 % 28 % 54.90 % 78 % 42.02 % 31.11 %
51.12 69.57 50 % 77.42 49.21 58.63 72 % 45.10 22 % 57.98 68.89
% % % % % % % %
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289
Table 2 Anterior X-ray: vertical exposition and surgical angles. Comparison between transnasal and transoral approaches Age (years)
Sex
Transoral approach: vertical exposition (cm)/surgical angle
Transnasal approach: vertical exposition (cm)/surgical angle
Vertical exposition (cm)
Surgical angle
Transnasal / transoral(%)
Percent superiority of transoral to transnasal
Transnasal / transoral(%)
Percent superiority of transoral to transnasal
90
F
ND
ND
ND
ND
ND
ND
56 80 79 98 55 94 51 42 75 69
M F F F M F M M M F
ND 4.930/124° 8.266/95° 6.866/138° 4.62/146° 6/156° 6.4/152° 6.533/158° 4.31/122° 4.55/140°
ND 1.533/26° 1.333/22° 1.544/40° 1.98/34° 1.2/22° 1.22/36° 1.133/21° 2.1/42° 2.24/39°
ND 31.09 16.12 22.48 42.85 20 % 19.06 17.34 48.72 49.23
ND 68.91 83.88 77.52 57.15 80 % 80.94 82.66 51.28 50.77
ND 20.96 23.15 28.98 23.28 14.10 23.68 13.29 34.42 27.85
ND 79.04 76.85 71.02 76.72 85.90 76.32 86.71 65.58 72.15
% % % % % % % %
% % % % % % % %
% % % % % % % % %
% % % % % % % % %
ND not determined
recommended in selected cases as a valid alternative to the transoral microscopic approach for the resection of the odontoid process of C2 and should be performed only by surgeons very skilled in endoscopic endonasal surgery and in endoscopic cadaver dissections [15]. The transoral endoscopic approach The 30-degree endoscope has been proposed for the transoral approach to avoid full soft-palate splitting, hard-palate splitting or extended maxillo/mandibulotomy [7, 9]. Using the endoscope, the operator is able to look in all directions by rotating the instrument. Because the light source is at the level of the abnormality, superior illumination can be obtained. With the aid of an endoscope, abnormalities as high as the mid-clivus can be visualised without extensive soft- or hard-palate manipulation [11, 16, 17].
The last high profile cadaveric study recently available in the literature is the one of Pillai et al. [11], which quantifies the surgical volume gained by this approach: the surgical area exposed over the posterior pharyngeal wall is significantly improved using the endoscope (606.5–127.4 mm3) compared with the operating microscope (425.7–100.8 mm3), without any compromise of surgical freedom (p = 0.05). The extent of the clivus exposed with the endoscope (9.5±0.7 mm) without splitting the soft palate is significantly improved compared with that associated with microscopic approach (2.0±0.4 mm) (p = 0.05) [11].
The present cadaveric study Our study on the cadaver is the first experience dealing with contextual neuroradiological “real time” examination and
Table 3 Transoral approach versus transnasal approach. Vertical and horizontal explorable distances and exposition angles Variable
Median (IQ range)
Minimum-maximum
SD
pa
Transoral approachb (vertical exposition, cm) Transnasal approach (vertical exposition, cm) Transoral approachb (vert. exposition angle) Transnasal approach (vert. exposition angle) Transoral approachc (horizontal exposition, cm) Transnasal approach (horizontal exposition, cm) Transoral approachc (horiz. exposition angle) Transnasal approach (horiz. exposition angle)
5.719 (1.365) 4.428 (2.960) 58 (13) 28 (17) 6.000 (2.115) 1.533 (0.830) 140 (31) 34 (18)
4.250–6.750 1.000–5.454 45–69 14–39 4.310–8.266 1.133–2.240 95–158 21–42
1.03 1.55 8.28 8.76 1.32 0.4 13.69 8.34
0.003
SD standard deviation a
Wilcoxon signed rank test
b
11 subjects
c
9 subjects
0.003 0.008 0.008
290
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Fig. 4 Median explorable distances (cm). Transoral vs transnasal approach
comparison of both transnasal and transoral CVJ surgical domains in the same subject. The impact of CVJ pathology is not addressed by this study; of course, cranial settling, CVJ kyphotic deformity and other changes will alter the relative utility of the two approaches. In fact, it must be pointed out that we studied only “normal” cadavers and, since the most common diseases found at this area are os odontoideum and basal invagination, in both circumstances, the tip of the dens is not easy to resect via the mouth. Moreover, different areas of exposure are not all of equal value for each operative goal and simple area or angle measurements cannot address this. Since the angles and distances are highly abstract for a surgeon and to know which Fig. 5 Median exposition angle (degrees). Transoral vs transnasal approach
anatomical structure can be reached with the two approaches, and which structures have to be destructed to reach the final target is mandatory, we used the NPL as ideal reference point to compare both surgical strategies. Nevertheless our study allows us to state that the transnasal approach, as it has already been widely discussed, is a viable strategy to reach the CVJ, but has limited angular (nostrils, choanae) and linear (NPL) surgical exposure, which in our view makes it suitable only for certain types of diseases and prevents its systematic applicability in other conditions, such as lateral tumours and pathologies caudal to C2. Although an obvious advantage of this approach is that there is no need to cut the soft palate, which minimises the potential postoperative morbidity like swallowing disturbances and
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hyper-nasal speech, which are really limiting to quality of life (lack palatine veil); the transoral approach provides a better exposure of the CVJ, both on the sagittal plane and on the transverse plane, providing a larger working channel and allowing an easier manoeuvrability of surgical instruments such as the endoscope [6]. With this tool, the advantage of the soft palate sparing might make the transnasal endoscopic approach less competitive compared with the transoral endoscopic assisted one. Finally, the potential for combining the two approaches to accomplish a particular surgical goal must be considered also a potential option. In our experience, we have used the endoscopic transoral route mainly in conjunction with the endoscopic transnasal approach to pathologies of the lower clivus such as chordomas. This shows that the two approaches are not competitive and can easily be used together to treat lesions that extend beyond the exposure limits of one or the other approach alone.
Conclusions Endoscopic endonasal and transoral approaches developed recently as promising alternatives to the classic microsurgical transoral approach to the CVJ (Table 4). From the pure anatomic point of view, our study seems to suggest that in normal conditions the transnasal approach to the CVJ is an oblique approach, which allows only the piecemeal removal of CVJ pathology and is not recommended for large tumours and low, and far laterally sited CVJ pathologies. The transnasal approach is limited in the caudal direction down to the NPL; otherwise the transoral approach is limited in the rostral direction with a maximum to the foramen magnum in a normal specimen. In every individual case, pros and cons of the appropriate approach have to be taken into account as well as the choice of a combined transnasal and transoral approach strategy.
Table 4 Transnasal and transoral: pros and cons of each approach Transnasal approach Pros: Partial isolation of the oral cavity, no needs of tracheostomy and reduced need of feeding tube. Cons: Oblique approach, only piecemeal removal of CVJ pathology is allowed, not recommended for large tumours and low sited CVJ pathologies. Transoral approach Pros: Direct approach, radical removal of huge tumours, good visualisation and comfortable mobilisation of surgical tools. Cons: Possible need of tracheostomy, need of feeding tube, difficult management of very high invagination conditions with platibasia.
291 Conflicts of interest None. Disclosure The authors declare no interest to disclose, they have any personal or institutional financial interest in drugs, materials or devices described in this submission and that they did not receive any specific funding.
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