C1-C2 Stabilization by Harms Arthrodesis: Indications, Technique

Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231

Available online at ScienceDirect www.sciencedirect.com

Original article

C1-C2 stabilization by harms arthrodesis: Indications, technique,

complications and outcomes in a prospective 26-case series

a a,∗ a a a,b

P. Bourdillon , G. Perrin , F. Lucas , R. Debarge , C. Barrey

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, France

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

a b s t r a c t

Article history: Introduction: C1-C2 arthrodesis is a surgical challenge due to the proximity of neurovascular structures

Accepted 27 September 2013

(vertebral arteries and spinal cord) and the wide range of motion of the joint, hampering bone fusion. A

variety of techniques have been successively recommended to reduce anatomic risk and improve results

Keywords: in terms of biomechanical stability and fusion rates. Recently, Harms described a new technique using

Harms

polyaxial screws in the C1 lateral masses and C2 pedicles.

C1-C2 fusion

Material and method: The present study reports our experience in a consecutive series of 26

Cervical fusion

patients operated on by C1-C2 arthrodesis using the Goel and Harms technique, and details techni-

C1-C2 instability

cal aspects step by step. Routine systematic immediate postoperative CT and 6-month CT controlled

C1-C2 screws

screw positioning and assessed fusion. Follow-up was at least 1 year, except in 2 cases (10

Cervical spine arthrodesis

months).

Results: 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 com-

plications and 85% of screws with perfect positioning) and an excellent rate of fusion (100% at 6

months).

Conclusion: Anatomic and biomechanical considerations, combined with the present clinical and radio-

logical outcomes, indicate that Goel and Harms fusion is to be considered the ﬁrst-line attitude of choice

for posterior C1-C2 arthrodesis.

Level of Evidence: Level IV prospective study.

1. Introduction Later, interlaminar hooks, with better biomechanical properties

than wiring, were introduced [6].

C1-C2 instability may have various causes, usually involving the Transarticular atlanto-axial screw ﬁxation, introduced by

C1-C2 axis or disc and ligamentary structures. Etiology is predomi- Magerl in 1986 [7], provided very high quality biomechanical sta-

nantly acute trauma, odontoid non-union, inﬂammatory pathology bility, with spectacularly improved fusion rates as compared to the

(rheumatoid arthritis) or tumor [1,2]. earlier posterior wiring techniques [8–12]. There were, however,

Atlanto-axial arthrodesis is technically demanding due to the several drawbacks, notably including the difﬁculty of performance

anatomic relations and wide range of motion of the joint, hin- in case of atlanto-axial dislocation or subluxation with loss of C1-C2

dering good-quality bone fusion [3]. Surgical C1-C2 fusion was alignment.

ﬁrst described by W. Gallie in 1939, and consisted in posterior In 2001, Harms developed Goel’s work on atlanto-axial screw

wiring [4], as subsequently developed by Brooks in the 1970s [5]. ﬁxation, describing a stabilization technique based on ﬁxation of

Biomechanical efﬁcacy, however, was limited and wiring served the C1 lateral masses and C2 isthmus using polyaxial screws [13].

more to maintain the interlaminar graft in position than to achieve Biomechanical results are comparable to those with Magerl’s tech-

real three-dimensional stability: a rigid cervical collar with 5 sup- nique [14,15] and surgery remains possible in case of posterior arc

ports and a frontal band was associated for a minimum 3 months. involvement (unlike with hook ﬁxation) or loss of C1-C2 alignment

(unlike with Magerl’s procedure).

The present report is of an original consecutive prospective

∗ series of 26 patients managed by cervical or occipito-cervical

Corresponding author.

arthrodesis including C1-C2, using the Harms technique.

E-mail address: [email protected] (G. Perrin).

226 P. Bourdillon et al. / Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231

Fig. 1. Screw entry points in C1 (left) and C2 (right).

2. Materials and methods A classic midline posterior cervical approach was performed,

exposing the spine from C0 to C3. Exposure had to be sufﬁciently

Patients aged over 18 years were consecutively included from lateral for the whole posterior arch of C2 and also the vertebral

January 1st, 2009 to January 1st, 2012. Minimum follow-up was 1 artery groove on the posterior arc of C1 to be visible. Particular care

year in all but 2 cases, in which it was for 10 months. was taken in dissecting the posterior arc of C1 to avoid vertebral

In all patients, posterior cervical arthrodesis including C1-C2 artery lesion (non-traumatic subperiosteal dissection).

was indicated consensually by the center’s spinal surgery team. The entry point for the C2 isthmus screw was at the junction

Inclusion was independent of etiology. of the superomedial and superolateral quadrants of the isthmus,

The following clinical data were analyzed: age, gender, etiol- slightly outside of the junction between the lamina and the facet

ogy of instability, operative time, blood loss, pre- and postoperative at mid-height of the posterior arch (Fig. 1). The screw-hole was

◦ ◦

neurological status, and complications (neurological, infectious and created using a 2.7 mm bit held about 30 upward and 20 con-

general). vergent. Lateral ﬂuoroscopic control allowed sagittal orientation

The following CT data were analyzed: cortical fracture (> 2 mm) to be adjusted. The diameter of the polyaxial Medtronic VERTEX

on immediate postoperative imaging, and rate of fusion on 6- C2 isthmus screw (Fig. 2) was usually 3.5 mm, with length ran-

month postoperative CT. Mechanical complications (displacement, ging between 18 and 30 mm depending on the patient’s anatomy

rupture of osteosynthesis material, screw detachment, etc.) were (whence the importance of pre-operative planning, with precise

collected from the two postoperative CT scans. measurement of the direction and diameter of the C2 isthmus).

C1-C2 fusion used polyaxial screws with a diameter of 3.5 mm The C2 root was systematically spared, being distracted down-

in C2 and 4 mm in C1, connected up by 3.2-mm titanium rods ward using an Olivecrona spatula, taking care to limit (usually by

(VERTEX, Medtronic , Minneapolis, MIN, USA), on either side inde- swabbing) bleeding of the venous plexuses that are very numerous

pendently. All patients were operated on by the same surgeon (CB), in this region.

to reduce variability related to surgical technique. The entry point for the C1 lateral mass lies at the intersection of a

sagittal axis through the middle of the C1-C2 joint and a transverse

2.1. Surgical technique axis through the junction of the posterior arc and the C1 lateral mass

(Fig. 3). Depending on its morphology, the posterior arc of C1 may

Patients were positioned prone, with a Mayﬁeld skull clamp, be partially rasped to facilitate screw placement. The screw-hole

◦

with the head held in neutral position or slight ﬂexion so as to is created using a 3 mm bit, with a slightly upward (20 ) and con-

◦

facilitate C1-C2 exposure. vergent (10 ) direction. Lateral ﬂuoroscopic control allows sagittal

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 the pedicle.

P. Bourdillon et al. / Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231 227

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 of

the C1 body is palpated by spatula.

Fig. 4. C1-C2 assembly following Harms (3D CT).

adjustment. Screw diameters were 4 mm, with length usually of 28 After radiological control, the posterior arcs were freshened

to 32 mm, depending on patient anatomy. Like for C2, the polyaxial under abundant irrigation using a large-diameter (4 or 5 mm) burr.

Medtronic VERTEX screw was used (Fig. 4). A large interlaminar graft was performed using decortication bone

After screw positioning, radiological control was repeated and 2 harvested during surgery associated to hydroxyapatite granules

Medtronic VERTEX rods were ﬁtted to connect the pairs of screws (Fig. 5).

on either side (Figs. 4 and 5). Additional distraction/compression

maneuver on the screws heads along the rod could be achieved to 3. Results

improve reduction and/or C1-C2 realignment.

Mean age was 57 years (SD, 19.3 years), with 16 male and 10

female patients (Table 1).

Eleven of the 26 patients (Fig. 6) presented odontoid fracture

non-union, 2 inﬂammatory pathologies (1 pannus on rheumatoid

arthritis, 1 gout), 11 trauma (fracture or severe C1-C2 sprain) and

2 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;

Fig. 5. Posterior arch freshening and interlaminar grafting. Fig. 6. Indications.

228 P. Bourdillon et al. / Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231

Table 1

Summary of indications, pre- and postoperative neurological status and operative data.

Age Gender Indication Preoperative Type of assembly Associated Postoperative Operative Blood loss neurological decompression neurological time

status status

Patient 1 81 M Non-union of odontoid Frankel C Harms C1-C2 C1 Frankel D 2 h 15 15 mL

fracture (4mm), facing laminectomy

odontoid granuloma

(type 2)

Patient 259M Complex C2 fracture, Frankel E Harms C1-C2 (left) and No Frankel E 3 h 50 50 mL

severe C1-C2 sprain transarticular (right).

Posterior graft, odontoid

screw ﬁxation

Patient 3 18 M Non-union of odontoid Frankel E Harms C1-C2, odontoid No Frankel E 3 h 50 400 mL

fracture (OBAR type 2) screw ﬁxation

Patient 473F Fracture of both C2 Frankel E Harms C1-C3, anterior No Frankel E1h 15 120 mL

lateral masses arthrodesis, posterior graft

Patient 5 84 M Odontoid non-union Frankel E Harms C1-C2, interlaminar No Frankel E 1 h 30 250 mL

(OBAR, type 2), graft

retro-odontoid pannus

Patient 671 F Non-union of odontoid Frankel E Harms C1-C2, interlaminar No Frankel E 2 h 15 890 mL

base fracture + graft

granuloma

Patient 7 25 M Fracture of C1 lateral Frankel E Harms C0-C1-C2, No Frankel E 2 h 45 410 mL

masses (congenital interlaminar graft

C0-C1 fusion)

Patient 8 51 M C0-C1 dislocation Frankel A Harms C0-C1-C2, No Frankel D 2 h 15 50 mL

interlaminar graft

Patient 9 77 F Non-union of odontoid Frankel E Harms C1-C2, interlaminar No Frankel E 1 h 30 160 mL

fracture (horizontal) graft

Patient 10 70 M Fracture of odontoid Frankel E Harms C1-C2, interlaminar No Frankel E 3 h 15 140 mL

base with 11 mm graft, odontoid screw

posterior displacement ﬁxation

Patient 11 33 M Bi-articular C2 fracture, Frankel E Harms C1-C3, interlaminar No Frankel E 1 h 30 90 mL

C2-C3 subluxation graft

Patient 12 60 F C1-C2 dislocation, Non- Harms C1-C2, interlaminar No Non- 1 h 45 250 mL

neurologic assessment assessable graft assessable

impossible (coma) (coma)

Patient 13 74 M Non-union of odontoid Frankel C Harms C1-C2 Laminectomy Frankel D 2 h 15 210 mL

fracture + pannus

Patient 14 27 M Traumatic C1-C2 Frankel D Harms C1-C2, interlaminar No Frankel E 2 h 00 240 mL

subluxation graft

Patient 15 65 F Pathologic fracture Frankel E C1 to C5 with C2 isthmus No Frankel E 4 h 50 300 mL

(complete C2 body screw ﬁxation, C2 and C4

lysis) cementoplasty

Patient 16 58 F Intracanal clivus Frankel E Harms C0-C4 (NB: right C1 No Frankel E 2 h 50 320 mL

chordoma and left C2 not screwed)

Patient 17 20 M Non-union of odontoid Frankel E Harms C1-C2 No Frankel E 2 h 30 250 mL

fracture (OBAR on Roy-Camille

classiﬁcation)

Patient 18 58 F C2-C3 dislocation Frankel E Harms C1-C3, C2-C3 cage No Frankel E 3 h 30 170 mL

fracture plate

Patient 19 36 F C1-C2 instability on Frankel E Harms C1-C2, interlaminar No Frankel E 2 h 15 150 mL

rheumatoid arthritis graft

Patient 20 60 M C1-C2 tophus (on gout) Frankel E Harms C1-C2 No Frankel E 2 h 45 220 mL

and odontoid fracture

Patient 21 58 F Fracture non-union Frankel E Harms C1-C2, odontoid No Frankel E 3 h 30 100 mL

(OBAR, type 2) screw ﬁxation

Patient 22 82 M Fracture non-union Frankel E Harms C1-C2, odontoid No Frankel E 4 h 00 850 mL

(OBAR, type 2) screw ﬁxation

Patient 23 64 M C2 Fracture non-union Frankel D + Harms C1-C2, interlaminar No Frankel E + 3 h 00 150 mL

(hook detachment) posterior graft resolution of cordonal posterior syndrome cordonal

syndrome

Patient 24 66 M Complex C2 fracture, Frankel A Harms C1-C3, interlaminar No Frankel A 2 h 30 400 mL

severe C1-C2 sprain graft

Patient 25 63 M Bipedicular C2 fracture Frankel E Harms C1-C3, interlaminar No Frankel E 2 h 00 320 mL

graft

Patient 26 57 M Anderson III C2 fracture Frankel E Harms C1-C3, odontoid No Frankel E 4 h 00 150 mL

screw ﬁxation,

interlaminar graft

P. Bourdillon et al. / Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231 229

Fig. 7. Pre- and postoperative neurologic status.

Fig. 9. Postoperative CT, assessing screw positioning.

range, 90–890 mL), taking all assemblies together. For 1-step Harms

4. Discussion

posterior C1-C2 assemblies, the mean ﬁgures were 130 min and

240 mL.

The present results are strictly in line with the literature

There was no postoperative neurological aggravation. Five of

[13,16,17]: an excellent rate of fusion, and very good reproducibil-

the 7 neurologically impaired patients showed clinical neurologi-

ity of correct screw positioning, testifying to the reliability of the

cal improvement (Fig. 7): 3 with non-union of an Anderson type-II technique.

fracture, and 2 with traumatic C1-C2 dislocation.

The fact that there were no cases of non-union or mechan-

Immediate postoperative radiological control, performed

ical complications in the present series conﬁrms the interest of

within 2 days of surgery, comprised thin-slice CT centered on C1-

this technique for achieving high-quality fusion. The early pos-

C2, with sagittal and coronal multiplanar reconstruction (Fig. 8). In

terior wiring techniques of C1-C2 arthrodesis, mentioned above,

2 cases, the scanner was not available in the intensive care setting,

achieved fusion in only two-thirds of cases [18,19] despite 3

and AP and lateral upper cervical spine X-rays were taken instead.

months’ cervical collar immobilization; the collars, moreover,

All screws were correctly positioned, with no cortical damage

incurred well-established speciﬁc morbidity such as delayed heal-

in most cases (22 out of 26: 85%). In the other 4 cases, the cortical

ing or operative site infection or scabbing (especially in elderly

fracture was less than 2 mm, without clinical impact; there were

subjects, who frequently show denutrition) and non-negligible

no fractures longer than 2 mm. Three of the 4 fractures were of the

psychological impact. Following Harms arthrodesis, we recom-

C0-C1 joint line, and the fourth of the transverse canal at C2 (with-

mend temporary (6 weeks) use of a supple collar when (and only

out vascular impact) (Figs. 9 and 10). No revision operations were

when) the cervical spine resumes load-bearing.

required and there were no clinical or radiological consequences

As in Harms’ own series of 37 patients [13], all of the screws

(notably vascular or neurological).

were more or less well positioned, and there were no vascular or

Patients were followed up at 6 months and 1 year. Systematic

neurologic lesions. We did, however, ﬁnd it wise to use short mono-

CT control at 6 months (Fig. 11) found no non-union or displace-

cortical and isthmus screws in C2, to minimize to risk of lesion to

ment of material. C1-C2 bone bridges were systematic, although of

the vertebral artery in its groove forward of the tip of the screw.

variable quality. Grafts were of poorer quality in case of C1 and/or

The main technical difﬁculty encountered concerned venous bleed-

C2 laminectomy, with smaller bone bridges.

ing due to the large number of plexuses around the C2 root and

Fig. 8. Postoperative CT, showing good screw positioning in a patient who received odontoid screw ﬁxation for complex displaced C1-C2 fracture.

230 P. Bourdillon et al. / Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231

Fig. 10. C1-C2 dislocation fracture (left). Day-2 postoperative CT (right) shows vertebral artery canal fracture on the left side.

facing the entry point on the C1 lateral mass. During exposure, Biomechanically, transarticular C1-C2 screw ﬁxation, as initially

these plexuses should be painstakingly distracted downward, pre- described with Magerl’s technique, provides much better stability

ventively, using 1 or 2 spatulas and hemostatic agents. In case of in both ﬂexion/extension and rotation than do wiring techniques

persistent bleeding, which is of venous origin, prolonged swabbing [8,20,21].

is usually effective. Also, due to the proximity of the C2 root, unpro- Stability has been compared between the Harms and Magerl

tected by any bony structure, bipolar forceps coagulation is to be techniques [8,17,22]: the two are equivalent; the Harms technique

preferred to monopolar sectioning. has the better biomechanical properties reported so far with pos-

Some authors recommend C2 root ligature, to promote terior C1-C2 arthrodesis. Given the potential technical difﬁculties

hemostasis; this is not, however, without clinical consequences of Magerl screw ﬁxation, especially when C1-C2 alignment is not

(hypoesthesia of the gonion and retroauricular region, associated conserved, and the greater risk of vertebral artery lesion (due to

with risk of neuralgia), and we consider the techniques described less convergent screw positioning), the Harms technique appears

above to be sufﬁciently effective in almost all cases. The quality of preferable. Associating posterior wiring to the Magerl technique,

the interlaminar grafts, moreover, is not such as to encourage C1-C2 as suggested by several teams in case of difﬁculty [11,23], does not

grafting sacriﬁcing the C2 root. seem indicated: it involves an intracanal step, increasing neurologic

C1-C2 hooks (linked by rods or clamps) avoid the risk of verte- risk for a biomechanical beneﬁt that has not been assessed.

bral artery lesion incurred by screwing, but have the disadvantage Certain authors have described a minimally invasive Harms pro-

of involving intracanal surgery (with supplementary neurologi- cedure [24]. Only 5 cases have as yet been reported, and beneﬁt and

cal risk) and cannot be used in case of laminar involvement (e.g., interest remain to be elucidated.

post-traumatic or secondary to laminectomy). Biomechanically, Navigation techniques have recently been described, and can

moreover, although laminar hooks provide anteroposterior sta- doubtless enhance reliability [25], especially in difﬁcult cases,

bility comparable to Magerl’s C1-C2 screw ﬁxation, stability in although the upper cervical spine is not the ideal site for navigation

rotation is much poorer [8]. The posterior interlaminar graft is also (limited exposure, deep operative site, mobile segment, etc.).

larger and more satisfactory when performed medially (between Taken together, the above arguments and present ﬁndings sug-

rods, as is the case in screwing) rather than laterally (as in hook gest to us that Harms fusion is the ﬁrst-line reference method for

ﬁxation, where it is lateral to the rods linking the hooks). posterior 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 6

months, with posterior bone graft remodelling.

P. Bourdillon et al. / Orthopaedics & Traumatology: Surgery & Research 100 (2014) 225–231 231

Disclosure of interest [11] Naderi S, Crawford NR, Song GS, Sonntag VK, Dickman CA. Biomechanical com-

parison of C1-C2 posterior ﬁxations. Cable, graft, and screw combinations. Spine

1998;23:1946–55.

The authors declare that they have no conﬂicts of interest con-

[12] Smith MD, Phillips WA, Hensinger RN. Complications of fusion to the upper

cerning this article. cervical spine. Spine 1991;16:702–5.

[13] Harms J, Melcher RP. Posterior C1-C2 fusion with polyaxial screw and rod

ﬁxation. Spine 2001;26:2467–71.

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