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Please cite this article in press as: Bourdillon P, et al. C1-C2 stabilization by harms arthrodesis: Indications, technique, complicationsand outcomes in a prospective 26-case series. Orthop Traumatol Surg Res (2014), http://dx.doi.org/10.1016/j.otsr.2013.09.019
ARTICLE IN PRESSG ModelOTSR 928 1–7
Orthopaedics & Traumatology: Surgery & Research xxx (2014) xxx–xxx
Available online at
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Original article
C1-C2 stabilization by harms arthrodesis: Indications, technique,complications and outcomes in a prospective 26-case series
P. Bourdillona,∗, G. Perrina, F. Lucasa, R. Debargea, C. Barreya,bQ1
a Service de Neurochirurgie C et Chirurgie du Rachis, Hôpital Pierre-Wertheimer, GHE, Hospices Civils de Lyon, Université Claude-Bernard Lyon 1, 59,boulevard Pinel, 69500 Bron, Franceb Laboratoire de Biomécanique, Art et Métiers Paristech, ESNAM, 151, boulevard de l’Hôpital, 75013 Paris, France
a r t i c l e i n f o
Article history:Accepted 27 September 2013
Keywords:HarmsC1-C2 fusionCervical fusionC1-C2 instabilityC1-C2 screwsCervical spine arthrodesis
a b s t r a c t
C1-C2 arthrodesis is a surgical challenge due to the proximity of neurovascular structures (vertebralarteries and spinal cord) and the wide range of motion of the joint, hampering bone fusion. A variety oftechniques have been successively recommended to reduce anatomic risk and improve results in termsof biomechanical stability and fusion rates. Recently, Harms described a new technique using polyaxialscrews in the C1 lateral masses and C2 pedicles. The present study reports our experience in a consecutiveseries of 26 patients operated on by C1-C2 arthrodesis using the Goel and Harms technique, and detailstechnical aspects step by step. Routine systematic immediate postoperative CT and 6-month CT controlledscrew positioning and assessed fusion. Follow-up was at least 1 year, except in 2 cases (10 months).Twenty-six patients with a mean age of 57 years were included. Indications comprised: C2 non-union(n = 11), C1-C2 fracture and/or dislocation (n = 11), inflammatory pathology (n = 2) and tumoral pathology(n = 2). The results showed the technique to be reliable (no neurovascular complications and 85% of screwswith perfect positioning) and an excellent rate of fusion (100% at 6 months). Anatomic and biomechanicalconsiderations, combined with the present clinical and radiological outcomes, indicate that Goel andHarms fusion is to be considered the first-line attitude of choice for posterior C1-C2 arthrodesis.Level of Evidence: Level IV prospective study.
© 2014 Published by Elsevier Masson SAS.
1. Introduction
C1-C2 instability may have various causes, usually involving theC1-C2 axis or disc and ligamentary structure. Etiology is predomi-nantly acute trauma, odontoid non-union, inflammatory pathology(rheumatoid arthritis) or tumor [1,2].
Atlanto-axial arthrodesis is technically demanding due to theanatomic relations and wide range of motion of the joint, hin-dering good-quality bone fusion [3]. Surgical C1-C2 fusion wasfirst described by W. Gallie in 1939, and consisted in posteriorwiring [4], as subsequently developed by Brooks in the 1970s [5].Biomechanical efficacy, however, was limited and wiring servedmore to maintain the interlaminar graft in position than to achievereal three-dimensional stability: a rigid cervical collar with 5 sup-ports and a frontal band was associated for a minimum 3 months.Later, interlaminar hooks, with better biomechanical propertiesthan wiring, were introduced [6].
Transarticular atlanto-axial screw fixation, introduced byMagerl in 1986 [7], provided very high quality biomechanical
∗ Corresponding author.E-mail address: [email protected] (P. Bourdillon).
stability, with spectacularly improved fusion rates as comparedto the earlier posterior wiring techniques [8–12]. There were,however, several drawbacks, notably including the difficulty of per-formance in case of atlanto-axial dislocation or subluxation withloss of C1-C2 alignment.
In 2001, Harms developed Goel’s work on atlanto-axial screwfixation, describing a stabilization technique based on fixation ofthe C1 lateral masses and C2 isthmus using polyaxial screws [13].Biomechanical results are comparable to those with Magerl’s tech-nique [14,15] and surgery remains possible in case of posterior arcinvolvement (unlike with hook fixation) or loss of C1-C2 alignment(unlike with Magerl’s procedure).
The present report is of an original consecutive prospectiveseries of 26 patients managed by cervical or occipito-cervicalarthrodesis including C1-C2, using the Harms technique.
2. Materials and methods
Patients aged over 18 years were consecutively included fromJanuary 1st, 2009 to January 1st, 2012. Minimum follow-up was 1year in all but 2 cases, in which it was for 10 months.
In all patients, posterior cervical arthrodesis including C1-C2was indicated consensually by the center’s spinal surgery team.
1877-0568/$ – see front matter © 2014 Published by Elsevier Masson SAS.http://dx.doi.org/10.1016/j.otsr.2013.09.019
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Please cite this article in press as: Bourdillon P, et al. C1-C2 stabilization by harms arthrodesis: Indications, technique, complicationsand outcomes in a prospective 26-case series. Orthop Traumatol Surg Res (2014), http://dx.doi.org/10.1016/j.otsr.2013.09.019
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Inclusion was independent of etiology.The following clinical data were analyzed: age, gender, etiol-
ogy of instability, operative time, blood loss, pre- and postoperativeneurological status, and complications (neurological, infectious andgeneral).
The following CT data were analyzed: cortical fracture(> 2 mm) on immediate postoperative imaging, and rate offusion on 6-month postoperative CT. Mechanical complications(displacement, rupture of osteosynthesis material, screw detach-ment, etc.) were collected from the two postoperative CTscans.
C1-C2 fusion used polyaxial screws with a diameter of 3.5 mmin C2 and 4 mm in C1, connected up by 3.2-mm titaniumrods (VERTEX, Medtronic®, Minneapolis, MIN, USA), on eitherside independently. All patients were operated on by the samesurgeon (CB), to reduce variability related to surgical tech-nique.
2.1. Surgical technique
Patients were positioned prone, with a Mayfield® skull clamp,with the head held in neutral position or slight flexion so as tofacilitate C1-C2 exposure.
A classic medial posterior cervical approach was performed,exposing the spine from C0 to C3. Exposure had to be sufficientlylateral for the whole of C2 and also the vertebral artery groove on
the posterior arc of C1 to be visible. Particular care was taken indissecting the posterior arc of C1 to avoid vertebral artery lesion(non-traumatic subperiosteal dissection).
The entry point for the C2 isthmus screw was at the junctionof the superomedial and superolateral quadrants of the isthmus,slightly outside of the junction between the lamina and the facet(Fig. 1). The screw-hole was created using a 2.7 mm bit heldabout 30◦ upward and 20◦ convergent. Lateral fluoroscopic con-trol allowed sagittal orientation to be adjusted. The diameter of thepolyaxial Medtronic® VERTEX C2 isthmus screw (Fig. 2) was usu-ally 3.5 mm, with length ranging between 18 and 30 mm dependingon the patient’s anatomy (whence the importance of pre-operativeplanning, with precise measurement of the direction and diameterof the C2 isthmus).
The C2 root was systematically spared, being distracted down-ward using an Olivecrona spatula, taking care to limit (usually byswabbing) bleeding of the venous plexuses that are very numerousin this region.
The entry point for the C1 lateral mass lies at the intersection of asagittal axis through the middle of the C1-C2 joint and a transverseaxis through the junction of the posterior arc and the C1 lateral mass(Fig. 3). Depending on its morphology, the posterior arc of C1 maybe partially rasped to facilitate screw placement. The screw-holeis created using a 3 mm bit, with a slightly upward (20◦) and con-vergent (10◦) direction. Lateral fluoroscopic control allows sagittaladjustment. Screw diameters were 4 mm, with length usually of 28
Fig. 1. Screw entry points in C1 (left) and C2 (right).
Fig. 2. Positioning of isthmus screws in C2. The medial edge of the pedicle is located and palpated with a spatula within the canal in contact with the medial side of thepedicle.
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Please cite this article in press as: Bourdillon P, et al. C1-C2 stabilization by harms arthrodesis: Indications, technique, complicationsand outcomes in a prospective 26-case series. Orthop Traumatol Surg Res (2014), http://dx.doi.org/10.1016/j.otsr.2013.09.019
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Fig. 3. Screw positioning in the left C1 lateral mass. Entry point exposure requires downward retraction of the venous plexuses and C2 root. The medial and lateral edges ofthe C1 body is palpated by spatula.
Fig. 4. C1-C2 assembly following Harms (3D CT).
to 32 mm, depending on patient anatomy. Like for C2, the polyaxialMedtronic® VERTEX screw was used (Fig. 4).
After screw positioning, radiological control was repeated and 2Medtronic® VERTEX rods were fitted to connect the pairs of screwson either side (Figs. 4 and 5).
After radiological control, the posterior arcs were freshenedunder abundant irrigation using a large-diameter (4 or 5 mm) burr.A large interlaminar graft was performed using decortication bone
Fig. 5. Posterior arch freshening and interlaminar grafting.
harvested during surgery associated to hydroxyapatite granules(Fig. 5).
3. Results
Mean age was 57 years (SD, 19.3 years), with 16 male and 10female patients (Table 1).
Eleven of the 26 patients (Fig. 6) presented odontoid fracturenon-union, 2 inflammatory pathologies (1 pannus on rheumatoidarthritis, 1 gout), 11 trauma (fracture or severe C1-C2 sprain) and2 tumors (1 chordoma, 1 odontoid metastasis).
Mean operative time was 160 minutes (SD, 53 min; range,1 h 15min–4 h 50 min) and mean blood loss 260 mL (SD, 203 mL;range, 90–890 mL), taking all assemblies together. For 1-step Harms
Fig. 6. Indications.
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Please cite this article in press as: Bourdillon P, et al. C1-C2 stabilization by harms arthrodesis: Indications, technique, complicationsand outcomes in a prospective 26-case series. Orthop Traumatol Surg Res (2014), http://dx.doi.org/10.1016/j.otsr.2013.09.019
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Table 1Summary of indications, pre- and postoperative neurological status and operative data.
Age Gender Indication Preoperativeneurologicalstatus
Type of assembly Associateddecompression
Postoperativeneurologicalstatus
Operativetime
Blood loss
Patient 1 81 M Non-union of odontoidfracture (4mm), facingodontoid granuloma(type 2)
Frankel C Harms C1-C2 C1laminectomy
Frankel D 2 h 15 15 mL
Patient 2 59 M Complex C2 fracture,severe C1-C2 sprain
Frankel E Harms C1-C2 (left) andtransarticular (right).Posterior graft, odontoidscrew fixation
No Frankel E 3 h 50 50 mL
Patient 3 18 M Non-union of odontoidfracture (OBAR type 2)
Frankel E Harms C1-C2, odontoidscrew fixation
No Frankel E 3 h 50 400 mL
Patient 4 73 F Fracture of both C2lateral masses
Frankel E Harms C1-C3, anteriorarthrodesis, posterior graft
No Frankel E 1 h 15 120 mL
Patient 5 84 M Odontoid non-union(OBAR, type 2),retro-odontoid pannus
Frankel E Harms C1-C2, interlaminargraft
No Frankel E 1 h 30 250 mL
Patient 6 71 F Non-union of odontoidbase fracture +granuloma
Frankel E Harms C1-C2, interlaminargraft
No Frankel E 2 h 15 890 mL
Patient 7 25 M Fracture of C1 lateralmasses (congenitalC0-C1 fusion)
Frankel E Harms C0-C1-C2,interlaminar graft
No Frankel E 2 h 45 410 mL
Patient 8 51 M C0-C1 dislocation Frankel A Harms C0-C1-C2,interlaminar graft
No Frankel D 2 h 15 50 mL
Patient 9 77 F Non-union of odontoidfracture (horizontal)
Frankel E Harms C1-C2, interlaminargraft
No Frankel E 1 h 30 160 mL
Patient 10 70 M Fracture of odontoidbase with 11 mmposterior displacement
Frankel E Harms C1-C2, interlaminargraft, odontoid screwfixation
No Frankel E 3 h 15 140 mL
Patient 11 33 M Bi-articular C2 fracture,C2-C3 subluxation
Frankel E Harms C1-C3, interlaminargraft
No Frankel E 1 h 30 90 mL
Patient 12 60 F C1-C2 dislocation,neurologic assessmentimpossible
Non-assessable(coma)
Harms C1-C2, interlaminargraft
No Non-assessable(coma)
1 h 45 250 mL
Patient 13 74 M Non-union of odontoidfracture + pannus
Frankel C Harms C1-C2 Laminectomy Frankel D 2 h 15 210 mL
Patient 14 27 M Traumatic C1-C2subluxation
Frankel D Harms C1-C2, interlaminargraft
No Frankel E 2 h 00 240 mL
Patient 15 65 F Pathologic fracture(complete C2 bodylysis)
Frankel E C1 to C5 with C2 isthmusscrew fixation, C2 and C4cementoplasty
No Frankel E 4 h 50 300 mL
Patient 16 58 F Intracanal clivuschordoma
Frankel E Harms C0-C4 (NB: right C1and left C2 not screwed)
No Frankel E 2 h 50 320 mL
Patient 17 20 M Non-union of odontoidfracture (OBAR onRoy-Camilleclassification)
Frankel E Harms C1-C2 No Frankel E 2 h 30 250 mL
Patient 18 58 F C2-C3 dislocationfracture
Frankel E Harms C1-C3, C2-C3 cageplate
No Frankel E 3 h 30 170 mL
Patient 19 36 F C1-C2 instability onrheumatoid arthritis
Frankel E Harms C1-C2, interlaminargraft
No Frankel E 2 h 15 150 mL
Patient 20 60 M C1-C2 tophus (on gout)and odontoid fracture
Frankel E Harms C1-C2 No Frankel E 2 h 45 220 mL
Patient 21 58 F Fracture non-union(OBAR, type 2)
Frankel E Harms C1-C2, odontoidscrew fixation
No Frankel E 3 h 30 100 mL
Patient 22 82 M Fracture non-union(OBAR, type 2)
Frankel E Harms C1-C2, odontoidscrew fixation
No Frankel E 4 h 00 850 mL
Patient 23 64 M C2 Fracture non-union(hook detachment)
Frankel D +posteriorcordonalsyndrome
Harms C1-C2, interlaminargraft
No Frankel E +resolution ofposteriorcordonalsyndrome
3 h 00 150 mL
Patient 24 66 M Complex C2 fracture,severe C1-C2 sprain
Frankel A Harms C1-C3, interlaminargraft
No Frankel A 2 h 30 400 mL
Patient 25 63 M Bipedicular C2 fracture Frankel E Harms C1-C3, interlaminargraft
No Frankel E 2 h 00 320 mL
Patient 26 57 M Anderson III C2 fracture Frankel E Harms C1-C3, odontoidscrew fixation,interlaminar graft
No Frankel E 4 h 00 150 mL
Please cite this article in press as: Bourdillon P, et al. C1-C2 stabilization by harms arthrodesis: Indications, technique, complicationsand outcomes in a prospective 26-case series. Orthop Traumatol Surg Res (2014), http://dx.doi.org/10.1016/j.otsr.2013.09.019
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Fig. 7. Pre- and postoperative neurologic status.
posterior C1-C2 assemblies, the mean figures were 130 min and240 mL.
There was no postoperative neurological aggravation. Five ofthe 7 neurologically impaired patients showed clinical neurologi-cal improvement (Fig. 7): 3 with non-union of an Anderson type-IIfracture, and 2 with traumatic C1-C2 dislocation.
Immediate postoperative radiological control, performedwithin 2 days of surgery, comprised thin-slice CT centered on C1-C2, with sagittal and coronal multiplanar reconstruction (Fig. 8).In 2 cases, the scanner was not available in the intensive caresetting, and AP and lateral upper cervical spine X-rays were takeninstead.
All screws were correctly positioned, with no cortical damagein most cases (22 out of 26: 85%). In the other 4 cases, the cor-tical fracture was less than 2 mm, without clinical impact; therewere no fractures longer than 2 mm. Three of the 4 fractureswere of the C0-C1 joint line, and the fourth of the transversecanal at C2 (without vascular impact) (Figs. 9 and 10). Norevision operations were required and there were no clinicalor radiological consequences (notably vascular or neurologi-cal).
Patients were followed up at 6 months and 1 year. SystematicCT control at 6 months (Fig. 11) found no non-union or displace-ment of material. C1-C2 bone bridges were systematic, although ofvariable quality. Grafts were of poorer quality in case of C1 and/orC2 laminectomy, with smaller bone bridges.
Fig. 9. Postoperative CT, assessing screw positioning.
4. Discussion
The present results are strictly in line with the literature[13,16,17]: an excellent rate of fusion, and very good reproducibil-ity of correct screw positioning, testifying to the reliability of thetechnique.
The fact that there were no cases of non-union or mechan-ical complications in the present series confirms the interest ofthis technique for achieving high-quality fusion. The early pos-terior wiring techniques of C1-C2 arthrodesis, mentioned above,achieved fusion in only two-thirds of cases [18,19] despite 3months’ cervical collar immobilization; the collars, moreover,incurred well-established specific morbidity such as delayed heal-ing or operative site infection or scabbing (especially in elderlysubjects, who frequently show denutrition) and non-negligiblepsychological impact. Following Harms arthrodesis, we recom-mend temporary (6 weeks) use of a supple collar when (and onlywhen) the cervical spine resumes load-bearing.
As in Harms’ own series of 37 patients [13], all of the screwswere more or less well positioned, and there were no vascular orneurologic lesions. We did, however, find it wise to use short mono-cortical and isthmus screws in C2, to minimize to risk of lesion tothe vertebral artery in its groove forward of the tip of the screw.The main technical difficulty encountered concerned venous bleed-ing due to the large number of plexuses around the C2 root andfacing the entry point on the C1 lateral mass. During exposure,
Fig. 8. Postoperative CT, showing good screw positioning in a patient who received odontoid screw fixation for complex displaced C1-C2 fracture.
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Please cite this article in press as: Bourdillon P, et al. C1-C2 stabilization by harms arthrodesis: Indications, technique, complicationsand outcomes in a prospective 26-case series. Orthop Traumatol Surg Res (2014), http://dx.doi.org/10.1016/j.otsr.2013.09.019
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Fig. 10. C1-C2 dislocation fracture (left). Day-2 postoperative CT (right) shows vertebral artery canal fracture on the left side.
these plexuses should be painstakingly distracted downward, pre-ventively, using 1 or 2 spatulas and hemostatic agents. In case ofpersistent bleeding, which is of venous origin, prolonged swabbingis usually effective. Also, due to the proximity of the C2 root, unpro-tected by any bony structure, bipolar forceps coagulation is to bepreferred to monopolar sectioning.
Some authors recommend C2 root ligature, to promotehemostasis; this is not, however, without clinical consequences(hypoesthesia of the gonion and retroauricular region, associatedwith risk of neuralgia), and we consider the techniques describedabove to be sufficiently effective in almost all cases. The quality ofthe interlaminar grafts, moreover, is not such as to encourage C1-C2grafting sacrificing the C2 root.
C1-C2 hooks (linked by rods or clamps) avoid the risk of verte-bral artery lesion incurred by screwing, but have the disadvantageof involving intracanal surgery (with supplementary neurologi-cal risk) and cannot be used in case of laminar involvement (e.g.,post-traumatic or secondary to laminectomy). Biomechanically,moreover, although laminar hooks provide anteroposterior sta-bility comparable to Magerl’s C1-C2 screw fixation, stability inrotation is much poorer [8]. The posterior interlaminar graft is alsolarger and more satisfactory when performed medially (betweenrods, as is the case in screwing) rather than laterally (as in hookfixation, where it is lateral to the rods linking the hooks).
Biomechanically, transarticular C1-C2 screw fixation, as initiallydescribed with Magerl’s technique, provides much better stability
in both flexion/extension and rotation than do wiring techniques[8,20,21].
Stability has been compared between the Harms and Magerltechniques [8,17,22]: the two are equivalent; the Harms tech-nique has the better biomechanical properties reported so far withposterior C1-C2 arthrodesis. Given the potential technical difficul-ties of Magerl screw fixation, especially when C1-C2 alignmentis not conserved, and the greater risk of vertebral artery lesion(due to less convergent screw positioning), the Harms techniqueappears preferable. Associating posterior wiring to the Magerl tech-nique, as suggested by several teams in case of difficulty [11,23],does not seem indicated: it involves an intracanal step, increas-ing neurologic risk for a biomechanical benefit that has not beenassessed.
Certain authors have described a minimally invasiveHarms procedure [24]. Only 5 cases have as yet beenreported, and benefit and interest remain to be eluci-dated.
Navigation techniques have recently been described, and candoubtless enhance reliability [25], especially in difficult cases,although the upper cervical spine is not the ideal site for nav-igation (limited exposure, deep operative site, mobile segment,etc.).
Taken together, the above arguments and present findings sug-gest to us that Harms fusion is the first-line reference method forposterior C1-C2 arthrodesis.
Fig. 11. Immediate postoperative (left) and 6-month (right) X-ray and CT control in a patient receiving Harms fusion with extension to C0. Excellent posterior fusion at 6months, with posterior bone graft remodelling.
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Disclosure of interest
The authors declare that they have no conflicts of interest con-cerning this article.
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