J Neurosurg Spine 21:761–768, 2014 ©AANS, 2014
Autologous clavicle bone graft for anterior cervical discectomy and fusion with titanium interbody cage Technical note Koichi Iwasaki, M.D.,1 Taichi Ikedo, M.D., 2 Hirokuni Hashikata, M.D.,1 and Hiroki Toda, M.D.1 Department of Neurosurgery, Kitano Medical Research Institute and Hospital, Osaka; and 2Department of Neurosurgery, Himeji Medical Center, Hyogo, Japan
1
A variety of donor-site complications have been reported for anterior cervical discectomy and fusion (ACDF) using autologous iliac bone graft. To minimize such morbidities and to obtain optimal bony fusion at the ACDF surgery, a novel technique was used to harvest cancellous bone from the autologous clavicle instead of the popular iliac crest graft. After a routine cervical discectomy of the affected level, a 1.5-cm linear skin incision was made over the clavicle within 2.5 cm of the sternoclavicular joint on the medial one-third portion. This portion is known as an anatomically safe zone, with no subcutaneous distribution of the supraclavicular nerve. Then, cancellous bone was harvested through a small cortical window developed on the clavicle. Care was taken not to injure the subclavian major vessels and the lung below the clavicle. A box-type titanium cage was packed with the harvested cancellous bone and then inserted into the discectomy-treated space for cervical interbody fusion. From 2009 to 2013, 16 patients with cervical radiculopathy and/or myelopathy underwent single-level ACDF with this method. All but 1 patient experienced significant improvement of clinical symptoms after the surgery and showed radiographic evidence of solid bony fusion and spinal stabilization within 6 months. Further, no peri- and postoperative complications at the clavicular donor site were noted. The mean visual analog scale pain score (range 0 [no pain to 10 [maximum pain]) at 1 year after the surgery was 0.1, and 13 of 14 patients with data at 1-year follow-up were highly satisfied with their donor-site cosmetic outcome. The clavicle is a safe, reliable, and technically easy source of autologous bone graft that yields optimal fusion rates and patient satisfaction with ACDF surgery. (http://thejns.org/doi/abs/10.3171/2014.7.SPINE131000)
Key Words • anterior cervical discectomy and fusion • autologous bone graft • clavicle • donor-site complications • iliac crest • titanium cage • technique
F
or anterior cervical discectomy and fusion (ACDF),
the iliac crest is the most popular source of autologous bone grafting.1,8,13 However, a variety of donor-site complications have been reported. These include postoperative persistent pain and paresthesia,16,17 lateral femoral cutaneous nerve injury, infection, hematoma, peritoneal perforation, visceral herniation, iliac fractures, and pelvic instability.2,7,12,15 The incidence of these morbidities is reportedly 10%–39%.2,7,12,15 To avoid the occurrence of such morbidities, some modified methods have been used to obtain autografts from alternative donor sites, including the sternum, fibula, patella, and rib.1,13,14 Such methods have not become popular probably because of unacceptable safety and reliability measures. Synthetic bone materials and cadaveric allografts have also been advocated as possible substitutes for autologous bones, but they may carry the risk of poor bony fusion, nonunion, and pathogen transmission.1,6,8,9,13 In this Abbreviations used in this paper: ACDF = anterior cervical discectomy and fusion; VAS = visual analog scale.
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report, we introduce a new method of using autologous cancellous bone obtained from the clavicle for ACDF, combined with an interbody cage, as a safe and reliable alternative to the conventional method. To the best of our knowledge, this is the first report to describe the clinical application of the clavicle bone for ACDF surgery.
Patient Profile
Methods
Between February 2009 and February 2013, 16 patients underwent this procedure (Table 1): 12 men and 4 women, ranging in age from 35 to 79 years. All patients presented with cervical radiculopathy and/or myelopathy and underwent single-level ACDF. The type of disorder included 11 (68.8%) cervical disc hernias, 2 (12.5%) degenerative osteophytes, 2 (12.5%) ossifying posterior longitudinal ligaments, and 1 (6.3%) spondylolisthesis. The affected level was C5–6 in 11 (68.8%) patients, C6–7 in 3 (18.8%) patients, and C3–4 in 2 (12.5%) patients. Clinical diagnosis and surgical indication were made after a 761
K. Iwasaki et al. TABLE 1: Summary of data obtained in 16 patients undergoing ACDF using autologous clavicle bone and titanium cage* Parameter age (yrs) mean range sex male female symptom myelopathy radiculopathy radiculomyelopathy disorder disc herniation osteophyte OPLL spondylolisthesis affected level C5–6 C6–7 C3–4 bone fusion rate (%) 2 mos 3 mos 6 mos
Value 60.0 35–79 12 4 10 3 3 11 2 2 1 11 3 2 0 25 100
* Values represent the number of patients, unless indicated otherwise. OPLL = ossification of the posterior longitudinal ligament; osteophyte = degenerative osteophyte.
total assessment of the preoperative neurological and radiological examinations. One patient (Case 6) was lost to follow-up at 6 months after the surgery. The postoperative follow-up period of the remaining 15 cases ranged from 12 months to 4 years (mean 32.3 months). The clinical details of each patient are shown in Table 2. Surgical Techniques
All patients were treated with a standard cervical discectomy using the modified Smith-Robinson technique18 and fusion with a titanium interbody cage packed with cancellous bone. The right side of the patient’s neck, including the upper chest region, was prepared and draped in one sterile operative field (Fig. 1A). After identification of the aimed level by x-ray fluoroscopy, a 3-cm linear skin incision was made on the front of the right side of the patient’s neck. Routine soft-tissue dissection and radical discectomy of the affected level were performed (Fig. 1B). A 1.5-cm horizontal skin incision was then made over the right clavicle within 2.5 cm of the sternoclavicular joint on the medial one-third portion, with care taken not to injure the medial branch of the supraclavicular nerve located lateral to the skin incision (Fig. 2A). The soft tissue and periosteum over the clavicle were dissected, and the super762
ficial aspect of the clavicle was exposed (Fig. 1C). Next, a small rectangular window (7 × 13 mm) was made on the cortex of the clavicle by using an oscillating bone saw, with careful attention not to injure the subclavian artery, the subclavian vein, and the apex of the lung (Figs. 1D and 2B). Through this cortical window, cancellous bone was harvested by using bone punches and curettes, with careful attention not to penetrate the posterior cortex of the clavicle (Figs. 1E and 2D). A box-type titanium cage (C-Varlock system, Kisco International) was packed with the harvested cancellous bone (Figs. 1F and 2C) and then inserted into the discectomy-treated space for cervical interbody fusion (Fig. 1G). The inner defect in the clavicle after harvesting was packed with Spongel (Astellas Pharma Inc.) for hemostasis, and the removed bone cortex was replaced in the original position, if possible (Fig. 2C). In all cases, the volume and quality of harvested cancellous bone were sufficient to occupy the inner cavity of the cage and to facilitate osseous fusion. Outcome Assessment
Radiological outcome was assessed using radiographs, CT scans, and MR images at 1 week and 1, 2, 3, 6, and 12 months after the surgery. Radiographic fusion was determined with dynamic radiographs to identify segment stability at the 2 vertebrae and with thin-section CT scans to identify the presence of bridging bone formation between the endplates of the fused vertebral bodies outside the cage and to ensure that there was no visible radiolucency around the cage. The postoperative state of the clavicle was also carefully followed to detect the occurrence of bone fracture, bone atrophy, or sternoclavicular joint instability. Clinical outcomes were investigated using the Odom criteria scale11 for neurological status and a visual analog scale (VAS) for donor-site wound pain, and patient’s satisfaction with the cosmetic wound appearance was also established. Odom criteria in each case were determined at the outpatient department at least 3 months after the surgery. Donor-site wound pain and patient satisfaction were assessed via a mail survey at 1 year after the surgery, using the modified methods of Heary et al.3 and Jagannathan et al., 5 respectively. The patients were asked to report VAS pain scores (range 0 [no pain] to 10 [maximum pain imaginable]) at 1 week, 1 month, and 1 year after the surgery and the degree of satisfaction (4-point scale: very satisfied, satisfied, minor complaints, dissatisfied) at 1 year after the surgery. Patients who did not respond to the mailed questionnaires were contacted via telephone and interviewed by a coordinator independent of the operating surgeons. At the time of the survey, 2 patients (Cases 4 and 6) could not be reached, resulting in 14 completed questionnaires (response rate 88%).
Surgical Results
Results
The mean operative duration was 120 minutes (range 90–140 minutes). Intraoperative blood loss was less than 50 ml in all patients. One patient (Case 3) with spondyloJ Neurosurg: Spine / Volume 21 / November 2014
Anterior cervical discectomy and fusion using clavicle bone TABLE 2: Clinical details in 16 patients undergoing ACDF using autologous clavicle bone and titanium cage* Postop Radiographic Fusion Case No.
Age (yrs), Sex
Diagnosis
Level
1 Mo
2 Mos
3 Mos
6 Mos
1 2 3† 4 5 6‡ 7 8 9 10 11 12 13 14 15 16
66, M 62, M 61, M 65, M 77, F 72, M 41, M 63, M 35, M 63, F 56, M 56, M 79, M 48, M 77, F 40, F
disc disc spondylolisthesis disc osteophyte disc disc OPLL disc disc disc OPLL disc disc osteophyte disc
C5–6 C5–6 C6–7 C5–6 C5–6 C3–4 C5–6 C5–6 C5–6 C5–6 C5–6 C5–6 C3–4 C5–6 C6–7 C6–7
no no no no no no no no no no no no no no no no
no no no no no no no no no no no no no no no no
no no no no no no yes no yes no no no no yes no yes
yes yes yes yes yes — yes yes yes yes yes yes yes yes yes yes
* disc = disc herniation. † Patient underwent additional stabilization with anterior plating system. ‡ Patient was lost to follow-up 6 months after the surgery.
listhesis after spinal trauma underwent additional stabilization with an anterior plate system after implantation of the cage. There were no major perioperative complications related to the ACDF procedure or harvesting of the graft, such as neurovascular injury, infection, or hematoma. As a minor complication, cerebrospinal fluid leak from the dural tear occurred in one patient (Case 8) due to the firm adhesion of the ossified posterior longitudinal ligaments to the dura. The leak point was successfully repaired using muscle fascia and fibrin glue. No patient required reoperation. Replacement of the removed bone cortex, intended to avoid skin dimpling and improve the cosmetic wound appearance, was performed in 5 cases. This procedure did not seem to influence the cosmetic outcome at followup within 6 months after the surgery, although long-term outcomes are as yet undetermined. Radiological Results
One patient (Case 6) was lost to follow-up at 6 months after the surgery. Bone fusion at 1, 2, 3, and 6 months after the surgery was observed in 0%, 0%, 25%, and 100% of the patients, respectively. All patients showed radiographic evidence of solid bony fusion and cervical stabilization within 6 months. In no case was pseudarthrosis, nonunion, cage displacement, or cervical instability observed. In one patient (Case 11), slight cage migration was observed 1 week after the surgery, but this was stabilized and resulted in complete fusion within 6 months after the surgery. Bone healing at the clavicular harvesting site was also uneventful; no complication, such as delayed bone fracture, bone atrophy, or sternoclavicular joint instability, was noted in any patient.
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Clinical Results
With respect to the functional outcome, all patients showed improvement of their clinical symptoms after the surgery. Odom criteria ratings for all patients are shown in Table 3. Data for 14 patients (response rate 88%) were available with regard to VAS score and patient satisfaction. Mean VAS pain scores at 1 week, 1 month, and 1 year after the surgery were 1.1, 0.8, and 0.1, respectively (Table 4). Thirteen patients (93%) declared no pain (VAS score of 0) at 1 year after the surgery. A high level of patient satisfaction with the cosmetic appearance of the donorsite wound was achieved with our method: 12 of the 14 patients (86%) were very satisfied with their cosmetic outcomes (Table 5).
Discussion
Combined use of autologous bone and a cage device is an effective method for ACDF. This technique can induce strong interbody osseous fusion and maintain spinal structural integrity, resulting in long-term cervical arthrodesis.4 Cages can facilitate mechanical strength to maintain disc height, and autologous cancellous bone plays a role in promoting graft incorporation and bony fusion due to new bone formation.4 It is important to pack sufficient volume of good-quality cancellous bone into the cage to induce early and optimal bone integration and fusion. The iliac crest has long been recognized among many spine surgeons as a reliable source for cancellous bone.1,8,13 However, the iliac crest is not an ideal donor site, because a variety of donorsite morbidities can result from its use.2,7,12,15–17 This has led 763
K. Iwasaki et al.
Fig. 1. Intraoperative photographs of ACDF using clavicle bone. A: The patient is placed in the supine position. A 3-cm linear skin incision (Line a) on the front of the right side of the neck and a 1.5-cm horizontal skin incision (Line b) on the medial one-third of the ipsilateral clavicle are designated within one sterile operative field. The line crossing Line a indicates the anterior margin of the sternocleidomastoid muscle. B: A standard cervical discectomy using the modified Smith-Robinson technique is then performed at the indicated disc space. C: The subcutaneous tissue and periosteum are divided over the superficial aspect of the clavicle. D: A small cortical window is made in a rectangular fashion (7 × 13 mm) using an oscillating bone saw. The black line (arrow) in C and D indicates the position of sternoclavicular joint. E: Cancellous bone is harvested through the small cortical window with a bone punch and a curette. F: The inner cavity of the cage, which is mounted on a cage holder, is packed with cancellous bone obtained from the patient’s clavicle. G: The cage is inserted into the discectomy-treated space for cervical interbody fusion.
to the search for other autologous donor sites.6,9 Cadaveric allografts and synthetic bone materials have been reported as alternatives to avoid harvesting autografts,6,8,9,14 but none are superior to autografts. Our own experience with donor-site morbidities and resultant patient dissatisfaction has prompted us to use the clavicle as an alternative source for cancellous bone. Based on a cadaveric study, Tubbs et al.19 suggested that the autologous clavicle might be a potential source for autograft in anterior cervical fusion. They harvested grafts from the thick segment of the middle one-third of the clavicle, and an average of 5 cm of bone was easily 764
removed with no gross injury to arteries and nerves. They also reported that there was no significant difference in length or diameter of the middle one-third of the clavicle based on gender or age. Compared with their method, in which the clavicular bone was harvested as a tricortical strut, our technique seems to be much safer and easier. In our method, we made a small cortical window on the clavicle surface and hollowed out only cancellous bone without touching the cortex of the ventral side. Therefore, the risk of a serious complication, such as injury to the underlying subclavian major vessels or lung, is considerably lower. The volume and quality of the cancellous bone J Neurosurg: Spine / Volume 21 / November 2014
Anterior cervical discectomy and fusion using clavicle bone
Fig. 2. Illustrations of the surgical procedures and the surrounding neurovascular structures. A: A 1.5-cm horizontal skin incision is made over the right clavicle within 2.5 cm of the sternoclavicular joint. This portion is a safe zone with no subcutaneous distribution of the supraclavicular nerve. B: After dividing the subcutaneous tissue and periosteum, a small cortical window is created in a rectangular fashion with an oscillating bone saw, with careful attention not to injure the subclavian large vessels and the lung. C: Cancellous bone is harvested through the cortical window and packed into a box-type titanium cage. Temporarily removed bone cortex is replaced in the original position, if possible. D: Careful curettage is required because the subclavian large vessels are located close to the cortex. Copyright Koichi Iwasaki. Published with permission.
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K. Iwasaki et al. TABLE 3: Outcome by Odom criteria ratings for all 16 patients Outcome
No. of Patients (%)
excellent good fair poor
9 (56) 6 (38) 1 (6) 0 (0)
harvested from the clavicle were sufficient to occupy the inner cavity of the interbody cages and to facilitate optimal osseous fusion. All patients in this series underwent single-level ACDF. To perform multilevel ACDF, it would be possible to harvest a larger volume of cancellous bone by creating a wider cortical window. Postoperative donor-site pain or paresthesia is one of the major factors influencing patient satisfaction. The reported incidence of chronic iliac donor-site pain ranges from 26% to 34%, with approximately 3%–10% patients reporting severe chronic pain.8,16,17 This high incidence may result from injury to the lateral femoral cutaneous nerve or its branch during iliac crest autograft harvesting. Thorough knowledge of a patient’s anatomy is required to avoid nerve injury. To investigate the nerve distribution on the clavicle area, Nathe et al.10 performed an anatomical dissection in 37 cadavers and found that there was a safe zone where no branch of the supraclavicular nerve was present within 2.7 cm of the sternoclavicular joint. The supraclavicular nerve provides sensation over the clavicle, anteromedial shoulder, and proximal chest, and injury to this nerve may result in pain, numbness, or discomfort in its distribution areas. In our method, we made a skin incision over the clavicle within 2.5 cm of the sternoclavicular joint, and no patients complained of chronic donor-site pain or paresthesia. Thus, Nathe et al.’s study supports the safety and the efficacy of our method of minimizing the risk of nerve injury that can cause sensory disturbance around the incision. With respect to wound appearance, high levels of patient satisfaction were obtained with our method: most patients were highly satisfied with the cosmetic appearance of the donor-site operative scar. An additional advantage of our method is the ability to perform both ACDF and bone harvest in a single operative field, which can save the time and labor needed to prepare separate fields.
TABLE 5: Patient satisfaction with the cosmetic wound appearance* Degree of Satisfaction
No. of Patients (%)
very satisfied satisfied minor complaints dissatisfied
12 (86) 1 (7) 1 (7)† 0 (0)
* Data for 14 patients were available (response rate 88%). † The patient in Case 15 reported mild irregularity of the wound surface.
tal with a 6-month history of progressive movement disorder of his left arm and fingers and slight gait disturbance after undergoing ineffective conservative treatments at another clinic. His symptoms had caused him to quit his job as a taxi driver. Neurological examination revealed Grade 3/5 weakness in extension and flexion of his wrist and fingers and an elevated deep tendon reflex of both lower limbs. Neuroradiological examinations disclosed a C5–6 disc herniation with severe compression of the spinal cord and the left C-6 nerve root (Fig. 3A and B). The patient underwent ACDF with the method reported here. His symptoms gradually improved after postoperative rehabilitation, and he returned to his original job 4 months after the surgery. His MR images immediately after the surgery showed complete removal of the herniated disc and appropriate decompression of the spinal cord (Fig. 3C and D). Follow-up x-rays and CT scans (Fig. 4A–E)
Representative Case
A 48-year-old man (Case 14) presented to our hospi-
TABLE 4: Outcome by average VAS pain score* Time After Surgery
VAS Score (range)†
1 wk 1 mo 1 yr
1.1 (0–5) 0.8 (0–4) 0.1 (0–2)
* Score range: 0 = no pain, 10 = maximum pain imaginable. † Mean based on 14 patients whose data were available (response rate: 88%).
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Fig. 3. A and B: Preoperative T2-weighted MR images of the representative case showing a disc herniation at the C5–6 level, with severe compression of the spinal cord and the left C-6 nerve root. C and D: Postoperative images showing complete removal of the herniated disc and appropriate decompression of the spinal cord and left C-6 root, although high intensity in the central cord remains.
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Anterior cervical discectomy and fusion using clavicle bone
Fig. 4. Thin-section CT scans (A, C, and D) and 3D reconstruction images (B and E), and a skin photograph of a representative case (F), at 1 week (A–C) and 6 months (D–F) after the surgery. A: Sagittal image showing the position of an inserted cage at the C5–6 level. Note that the cleavage between the vertebral endplates and packed cancellous bone (arrows) is clearly visualized. B: 3D image demonstrating an inserted cage with faint metal artifact and a small rectangular bone window (asterisk) on the right clavicle. C: Axial image at the level of the right clavicle showing the radiolucent area (asterisk) under a small bone window indicating the bone defect after harvesting cancellous bone. D: Sagittal view revealing bone bridge formation (arrows) between both the endplates that has completely incorporated the cage. Note that the cleavage between the vertebral endplates and cancellous bone is obscure. E: 3D image showing that new bone formation (arrows) outside the cage has completely covered the surface of the cage and that healing of the donor site on the clavicle has also been completed. F: Photograph showing the appearance of the skin 6 months after surgery. There are 2 smooth and nearly unnoticeable surgical scars (arrows).
showed gradual development of bony fusion and spinal stability of the operated segment, finally resulting in rigid arthrodesis within 6 months after the surgery. Healing and cosmetic appearance of the both surgical wounds were uneventful, and the patient did not complain of pain or other morbidities at the donor site (Fig. 4F).
Conclusions
Compared with conventional ACDF using autologous iliac bone, our new method has the advantage of reducing donor-site morbidities; it also achieves a high level of patient satisfaction with the cosmetic appearance of the postoperative scars. Furthermore, high rates of bony fusion and cervical stabilization are achieved. To the best of our knowledge, this is the first report of the clinical use of clavicular bone for ACDF surgery. Acknowledgment We thank Norikazu Yamana, M.D., Department of Neurosurgery, Himeji Medical Center, Hyogo, Japan, for his kind assistance in data collection.
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Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Iwasaki. Acquisition of data: Iwasaki, Ikedo. Analysis and interpretation of data: Iwasaki, Hashikata. Drafting the article: Iwasaki. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Iwasaki. Study supervision: Iwasaki. References 1. Chau AM, Mobbs RJ: Bone graft substitutes in anterior cervical discectomy and fusion. Eur Spine J 18:449–464, 2009 2. Fowler BL, Dall BE, Rowe DE: Complications associated with harvesting autogenous iliac bone graft. Am J Orthop 24: 895–903, 1995 3. Heary RF, Schlenk RP, Sacchieri TA, Barone D, Brotea C: Persistent iliac crest donor site pain: independent outcome assessment. Neurosurgery 50:510–517, 2002 4. Hwang SL, Hwang YF, Lieu AS, Lin CL, Kuo TH, Su YF, et al: Outcome analyses of interbody titanium cage fusion used
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K. Iwasaki et al. in the anterior discectomy for cervical degenerative disc disease. J Spinal Disord Tech 18:326–331, 2005 5. Jagannathan J, Chankaew E, Urban P, Dumont AS, Sansur CA, Kern J, et al: Cosmetic and functional outcomes following paramedian and anterolateral retroperitoneal access in anterior lumbar spine surgery. Clinical article. J Neurosurg Spine 9:454–465, 2008 6. Jensen WK, Moore TA, Tribus CB, Anderson PA, Zdeblick TA: Use of patella allograft for anterior cervical diskectomy and fusion. J Spinal Disord Tech 22:392–398, 2009 7. Kurz LT, Garfin SR, Booth RE Jr: Harvesting autogenous iliac bone grafts. A review of complications and techniques. Spine (Phila Pa 1976) 14:1324–1331, 1989 8. Lebow R, Yao T, Stevenson CB, Cheng JS: Bone graft options, bone graft substitutes, and bone harvest techniques, in Winn HR (ed): Youmans Neurological Surgery, ed 6. Philadelphia: Elsevier, 2011, Vol 3, pp 2992–2998 9. Martin GJ Jr, Haid RW Jr, MacMillan M, Rodts GE Jr, Berkman R: Anterior cervical discectomy with freeze-dried fibula allograft. Overview of 317 cases and literature review. Spine (Phila Pa 1976) 24:852–859, 1999 10. Nathe T, Tseng S, Yoo B: The anatomy of the supraclavicular nerve during surgical approach to the clavicular shaft. Clin Orthop Relat Res 469:890–894, 2011 11. Odom GL, Finney W, Woodhall B: Cervical disk lesions. J Am Med Assoc 166:23–28, 1958 12. Pollock R, Alcelik I, Bhatia C, Chuter G, Lingutla K, Budithi C, et al: Donor site morbidity following iliac crest bone harvesting for cervical fusion: a comparison between minimally invasive and open techniques. Eur Spine J 17:845–852, 2008 13. Ryken TC, Heary RF, Matz PG, Anderson PA, Groff MW, Holly LT, et al: Techniques for cervical interbody grafting. J Neurosurg Spine 11:203–220, 2009
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14. Sangala JR, Nichols T, Uribe JS, Melton M, Vale FL: Sternal cancellous bone graft harvest for anterior cervical discectomy and fusion with interbody cage devices. Clin Neurol Neurosurg 112:470–473, 2010 15. Seiler JG III, Johnson J: Iliac crest autogenous bone grafting: donor site complications. J South Orthop Assoc 9:91–97, 2000 16. Shamsaldin M, Mouchaty H, Desogus N, Costagliola C, Di Lorenzo N: Evaluation of donor site pain after anterior iliac crest harvesting for cervical fusion: a prospective study on 50 patients. Acta Neurochir (Wien) 148:1071–1074, 2006 17. Skeppholm M, Olerud C: Pain from donor site after anterior cervical fusion with bone graft: a prospective randomized study with 12 months of follow-up. Eur Spine J 22:142–147, 2013 18. Smith GW, Robinson RA: The treatment of certain cervicalspine disorders by anterior removal of the intervertebral disc and interbody fusion. J Bone Joint Surg Am 40-A:607–624, 1958 19. Tubbs RS, Louis RG Jr, Wartmann CT, Cormier JL, Pearson BE, Loukas M, et al: Use of the clavicle in anterior cervical discectomy/corpectomy fusion procedures: cadaveric feasibility study. Childs Nerv Syst 24:337–341, 2008
Manuscript submitted November 5, 2013. Accepted July 21, 2014. Please include this information when citing this paper: published online August 29, 2014; DOI: 10.3171/2014.7.SPINE131000. Address correspondence to: Koichi Iwasaki, M.D., Department of Neurosurgery, Kitano Medical Research Institute and Hospital, 2-4-20 Ogi-machi, Kita-ku, Osaka 530-8480, Japan. email: todaiji [email protected].
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Autologous clavicle bone graft for anterior cervical discectomy and fusion with titanium interbody cage Technical note Koichi Iwasaki, M.D.,1 Taichi Ikedo, M.D., 2 Hirokuni Hashikata, M.D.,1 and Hiroki Toda, M.D.1 Department of Neurosurgery, Kitano Medical Research Institute and Hospital, Osaka; and 2Department of Neurosurgery, Himeji Medical Center, Hyogo, Japan
1
A variety of donor-site complications have been reported for anterior cervical discectomy and fusion (ACDF) using autologous iliac bone graft. To minimize such morbidities and to obtain optimal bony fusion at the ACDF surgery, a novel technique was used to harvest cancellous bone from the autologous clavicle instead of the popular iliac crest graft. After a routine cervical discectomy of the affected level, a 1.5-cm linear skin incision was made over the clavicle within 2.5 cm of the sternoclavicular joint on the medial one-third portion. This portion is known as an anatomically safe zone, with no subcutaneous distribution of the supraclavicular nerve. Then, cancellous bone was harvested through a small cortical window developed on the clavicle. Care was taken not to injure the subclavian major vessels and the lung below the clavicle. A box-type titanium cage was packed with the harvested cancellous bone and then inserted into the discectomy-treated space for cervical interbody fusion. From 2009 to 2013, 16 patients with cervical radiculopathy and/or myelopathy underwent single-level ACDF with this method. All but 1 patient experienced significant improvement of clinical symptoms after the surgery and showed radiographic evidence of solid bony fusion and spinal stabilization within 6 months. Further, no peri- and postoperative complications at the clavicular donor site were noted. The mean visual analog scale pain score (range 0 [no pain to 10 [maximum pain]) at 1 year after the surgery was 0.1, and 13 of 14 patients with data at 1-year follow-up were highly satisfied with their donor-site cosmetic outcome. The clavicle is a safe, reliable, and technically easy source of autologous bone graft that yields optimal fusion rates and patient satisfaction with ACDF surgery. (http://thejns.org/doi/abs/10.3171/2014.7.SPINE131000)
Key Words • anterior cervical discectomy and fusion • autologous bone graft • clavicle • donor-site complications • iliac crest • titanium cage • technique
F
or anterior cervical discectomy and fusion (ACDF),
the iliac crest is the most popular source of autologous bone grafting.1,8,13 However, a variety of donor-site complications have been reported. These include postoperative persistent pain and paresthesia,16,17 lateral femoral cutaneous nerve injury, infection, hematoma, peritoneal perforation, visceral herniation, iliac fractures, and pelvic instability.2,7,12,15 The incidence of these morbidities is reportedly 10%–39%.2,7,12,15 To avoid the occurrence of such morbidities, some modified methods have been used to obtain autografts from alternative donor sites, including the sternum, fibula, patella, and rib.1,13,14 Such methods have not become popular probably because of unacceptable safety and reliability measures. Synthetic bone materials and cadaveric allografts have also been advocated as possible substitutes for autologous bones, but they may carry the risk of poor bony fusion, nonunion, and pathogen transmission.1,6,8,9,13 In this Abbreviations used in this paper: ACDF = anterior cervical discectomy and fusion; VAS = visual analog scale.
J Neurosurg: Spine / Volume 21 / November 2014
report, we introduce a new method of using autologous cancellous bone obtained from the clavicle for ACDF, combined with an interbody cage, as a safe and reliable alternative to the conventional method. To the best of our knowledge, this is the first report to describe the clinical application of the clavicle bone for ACDF surgery.
Patient Profile
Methods
Between February 2009 and February 2013, 16 patients underwent this procedure (Table 1): 12 men and 4 women, ranging in age from 35 to 79 years. All patients presented with cervical radiculopathy and/or myelopathy and underwent single-level ACDF. The type of disorder included 11 (68.8%) cervical disc hernias, 2 (12.5%) degenerative osteophytes, 2 (12.5%) ossifying posterior longitudinal ligaments, and 1 (6.3%) spondylolisthesis. The affected level was C5–6 in 11 (68.8%) patients, C6–7 in 3 (18.8%) patients, and C3–4 in 2 (12.5%) patients. Clinical diagnosis and surgical indication were made after a 761
K. Iwasaki et al. TABLE 1: Summary of data obtained in 16 patients undergoing ACDF using autologous clavicle bone and titanium cage* Parameter age (yrs) mean range sex male female symptom myelopathy radiculopathy radiculomyelopathy disorder disc herniation osteophyte OPLL spondylolisthesis affected level C5–6 C6–7 C3–4 bone fusion rate (%) 2 mos 3 mos 6 mos
Value 60.0 35–79 12 4 10 3 3 11 2 2 1 11 3 2 0 25 100
* Values represent the number of patients, unless indicated otherwise. OPLL = ossification of the posterior longitudinal ligament; osteophyte = degenerative osteophyte.
total assessment of the preoperative neurological and radiological examinations. One patient (Case 6) was lost to follow-up at 6 months after the surgery. The postoperative follow-up period of the remaining 15 cases ranged from 12 months to 4 years (mean 32.3 months). The clinical details of each patient are shown in Table 2. Surgical Techniques
All patients were treated with a standard cervical discectomy using the modified Smith-Robinson technique18 and fusion with a titanium interbody cage packed with cancellous bone. The right side of the patient’s neck, including the upper chest region, was prepared and draped in one sterile operative field (Fig. 1A). After identification of the aimed level by x-ray fluoroscopy, a 3-cm linear skin incision was made on the front of the right side of the patient’s neck. Routine soft-tissue dissection and radical discectomy of the affected level were performed (Fig. 1B). A 1.5-cm horizontal skin incision was then made over the right clavicle within 2.5 cm of the sternoclavicular joint on the medial one-third portion, with care taken not to injure the medial branch of the supraclavicular nerve located lateral to the skin incision (Fig. 2A). The soft tissue and periosteum over the clavicle were dissected, and the super762
ficial aspect of the clavicle was exposed (Fig. 1C). Next, a small rectangular window (7 × 13 mm) was made on the cortex of the clavicle by using an oscillating bone saw, with careful attention not to injure the subclavian artery, the subclavian vein, and the apex of the lung (Figs. 1D and 2B). Through this cortical window, cancellous bone was harvested by using bone punches and curettes, with careful attention not to penetrate the posterior cortex of the clavicle (Figs. 1E and 2D). A box-type titanium cage (C-Varlock system, Kisco International) was packed with the harvested cancellous bone (Figs. 1F and 2C) and then inserted into the discectomy-treated space for cervical interbody fusion (Fig. 1G). The inner defect in the clavicle after harvesting was packed with Spongel (Astellas Pharma Inc.) for hemostasis, and the removed bone cortex was replaced in the original position, if possible (Fig. 2C). In all cases, the volume and quality of harvested cancellous bone were sufficient to occupy the inner cavity of the cage and to facilitate osseous fusion. Outcome Assessment
Radiological outcome was assessed using radiographs, CT scans, and MR images at 1 week and 1, 2, 3, 6, and 12 months after the surgery. Radiographic fusion was determined with dynamic radiographs to identify segment stability at the 2 vertebrae and with thin-section CT scans to identify the presence of bridging bone formation between the endplates of the fused vertebral bodies outside the cage and to ensure that there was no visible radiolucency around the cage. The postoperative state of the clavicle was also carefully followed to detect the occurrence of bone fracture, bone atrophy, or sternoclavicular joint instability. Clinical outcomes were investigated using the Odom criteria scale11 for neurological status and a visual analog scale (VAS) for donor-site wound pain, and patient’s satisfaction with the cosmetic wound appearance was also established. Odom criteria in each case were determined at the outpatient department at least 3 months after the surgery. Donor-site wound pain and patient satisfaction were assessed via a mail survey at 1 year after the surgery, using the modified methods of Heary et al.3 and Jagannathan et al., 5 respectively. The patients were asked to report VAS pain scores (range 0 [no pain] to 10 [maximum pain imaginable]) at 1 week, 1 month, and 1 year after the surgery and the degree of satisfaction (4-point scale: very satisfied, satisfied, minor complaints, dissatisfied) at 1 year after the surgery. Patients who did not respond to the mailed questionnaires were contacted via telephone and interviewed by a coordinator independent of the operating surgeons. At the time of the survey, 2 patients (Cases 4 and 6) could not be reached, resulting in 14 completed questionnaires (response rate 88%).
Surgical Results
Results
The mean operative duration was 120 minutes (range 90–140 minutes). Intraoperative blood loss was less than 50 ml in all patients. One patient (Case 3) with spondyloJ Neurosurg: Spine / Volume 21 / November 2014
Anterior cervical discectomy and fusion using clavicle bone TABLE 2: Clinical details in 16 patients undergoing ACDF using autologous clavicle bone and titanium cage* Postop Radiographic Fusion Case No.
Age (yrs), Sex
Diagnosis
Level
1 Mo
2 Mos
3 Mos
6 Mos
1 2 3† 4 5 6‡ 7 8 9 10 11 12 13 14 15 16
66, M 62, M 61, M 65, M 77, F 72, M 41, M 63, M 35, M 63, F 56, M 56, M 79, M 48, M 77, F 40, F
disc disc spondylolisthesis disc osteophyte disc disc OPLL disc disc disc OPLL disc disc osteophyte disc
C5–6 C5–6 C6–7 C5–6 C5–6 C3–4 C5–6 C5–6 C5–6 C5–6 C5–6 C5–6 C3–4 C5–6 C6–7 C6–7
no no no no no no no no no no no no no no no no
no no no no no no no no no no no no no no no no
no no no no no no yes no yes no no no no yes no yes
yes yes yes yes yes — yes yes yes yes yes yes yes yes yes yes
* disc = disc herniation. † Patient underwent additional stabilization with anterior plating system. ‡ Patient was lost to follow-up 6 months after the surgery.
listhesis after spinal trauma underwent additional stabilization with an anterior plate system after implantation of the cage. There were no major perioperative complications related to the ACDF procedure or harvesting of the graft, such as neurovascular injury, infection, or hematoma. As a minor complication, cerebrospinal fluid leak from the dural tear occurred in one patient (Case 8) due to the firm adhesion of the ossified posterior longitudinal ligaments to the dura. The leak point was successfully repaired using muscle fascia and fibrin glue. No patient required reoperation. Replacement of the removed bone cortex, intended to avoid skin dimpling and improve the cosmetic wound appearance, was performed in 5 cases. This procedure did not seem to influence the cosmetic outcome at followup within 6 months after the surgery, although long-term outcomes are as yet undetermined. Radiological Results
One patient (Case 6) was lost to follow-up at 6 months after the surgery. Bone fusion at 1, 2, 3, and 6 months after the surgery was observed in 0%, 0%, 25%, and 100% of the patients, respectively. All patients showed radiographic evidence of solid bony fusion and cervical stabilization within 6 months. In no case was pseudarthrosis, nonunion, cage displacement, or cervical instability observed. In one patient (Case 11), slight cage migration was observed 1 week after the surgery, but this was stabilized and resulted in complete fusion within 6 months after the surgery. Bone healing at the clavicular harvesting site was also uneventful; no complication, such as delayed bone fracture, bone atrophy, or sternoclavicular joint instability, was noted in any patient.
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Clinical Results
With respect to the functional outcome, all patients showed improvement of their clinical symptoms after the surgery. Odom criteria ratings for all patients are shown in Table 3. Data for 14 patients (response rate 88%) were available with regard to VAS score and patient satisfaction. Mean VAS pain scores at 1 week, 1 month, and 1 year after the surgery were 1.1, 0.8, and 0.1, respectively (Table 4). Thirteen patients (93%) declared no pain (VAS score of 0) at 1 year after the surgery. A high level of patient satisfaction with the cosmetic appearance of the donorsite wound was achieved with our method: 12 of the 14 patients (86%) were very satisfied with their cosmetic outcomes (Table 5).
Discussion
Combined use of autologous bone and a cage device is an effective method for ACDF. This technique can induce strong interbody osseous fusion and maintain spinal structural integrity, resulting in long-term cervical arthrodesis.4 Cages can facilitate mechanical strength to maintain disc height, and autologous cancellous bone plays a role in promoting graft incorporation and bony fusion due to new bone formation.4 It is important to pack sufficient volume of good-quality cancellous bone into the cage to induce early and optimal bone integration and fusion. The iliac crest has long been recognized among many spine surgeons as a reliable source for cancellous bone.1,8,13 However, the iliac crest is not an ideal donor site, because a variety of donorsite morbidities can result from its use.2,7,12,15–17 This has led 763
K. Iwasaki et al.
Fig. 1. Intraoperative photographs of ACDF using clavicle bone. A: The patient is placed in the supine position. A 3-cm linear skin incision (Line a) on the front of the right side of the neck and a 1.5-cm horizontal skin incision (Line b) on the medial one-third of the ipsilateral clavicle are designated within one sterile operative field. The line crossing Line a indicates the anterior margin of the sternocleidomastoid muscle. B: A standard cervical discectomy using the modified Smith-Robinson technique is then performed at the indicated disc space. C: The subcutaneous tissue and periosteum are divided over the superficial aspect of the clavicle. D: A small cortical window is made in a rectangular fashion (7 × 13 mm) using an oscillating bone saw. The black line (arrow) in C and D indicates the position of sternoclavicular joint. E: Cancellous bone is harvested through the small cortical window with a bone punch and a curette. F: The inner cavity of the cage, which is mounted on a cage holder, is packed with cancellous bone obtained from the patient’s clavicle. G: The cage is inserted into the discectomy-treated space for cervical interbody fusion.
to the search for other autologous donor sites.6,9 Cadaveric allografts and synthetic bone materials have been reported as alternatives to avoid harvesting autografts,6,8,9,14 but none are superior to autografts. Our own experience with donor-site morbidities and resultant patient dissatisfaction has prompted us to use the clavicle as an alternative source for cancellous bone. Based on a cadaveric study, Tubbs et al.19 suggested that the autologous clavicle might be a potential source for autograft in anterior cervical fusion. They harvested grafts from the thick segment of the middle one-third of the clavicle, and an average of 5 cm of bone was easily 764
removed with no gross injury to arteries and nerves. They also reported that there was no significant difference in length or diameter of the middle one-third of the clavicle based on gender or age. Compared with their method, in which the clavicular bone was harvested as a tricortical strut, our technique seems to be much safer and easier. In our method, we made a small cortical window on the clavicle surface and hollowed out only cancellous bone without touching the cortex of the ventral side. Therefore, the risk of a serious complication, such as injury to the underlying subclavian major vessels or lung, is considerably lower. The volume and quality of the cancellous bone J Neurosurg: Spine / Volume 21 / November 2014
Anterior cervical discectomy and fusion using clavicle bone
Fig. 2. Illustrations of the surgical procedures and the surrounding neurovascular structures. A: A 1.5-cm horizontal skin incision is made over the right clavicle within 2.5 cm of the sternoclavicular joint. This portion is a safe zone with no subcutaneous distribution of the supraclavicular nerve. B: After dividing the subcutaneous tissue and periosteum, a small cortical window is created in a rectangular fashion with an oscillating bone saw, with careful attention not to injure the subclavian large vessels and the lung. C: Cancellous bone is harvested through the cortical window and packed into a box-type titanium cage. Temporarily removed bone cortex is replaced in the original position, if possible. D: Careful curettage is required because the subclavian large vessels are located close to the cortex. Copyright Koichi Iwasaki. Published with permission.
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K. Iwasaki et al. TABLE 3: Outcome by Odom criteria ratings for all 16 patients Outcome
No. of Patients (%)
excellent good fair poor
9 (56) 6 (38) 1 (6) 0 (0)
harvested from the clavicle were sufficient to occupy the inner cavity of the interbody cages and to facilitate optimal osseous fusion. All patients in this series underwent single-level ACDF. To perform multilevel ACDF, it would be possible to harvest a larger volume of cancellous bone by creating a wider cortical window. Postoperative donor-site pain or paresthesia is one of the major factors influencing patient satisfaction. The reported incidence of chronic iliac donor-site pain ranges from 26% to 34%, with approximately 3%–10% patients reporting severe chronic pain.8,16,17 This high incidence may result from injury to the lateral femoral cutaneous nerve or its branch during iliac crest autograft harvesting. Thorough knowledge of a patient’s anatomy is required to avoid nerve injury. To investigate the nerve distribution on the clavicle area, Nathe et al.10 performed an anatomical dissection in 37 cadavers and found that there was a safe zone where no branch of the supraclavicular nerve was present within 2.7 cm of the sternoclavicular joint. The supraclavicular nerve provides sensation over the clavicle, anteromedial shoulder, and proximal chest, and injury to this nerve may result in pain, numbness, or discomfort in its distribution areas. In our method, we made a skin incision over the clavicle within 2.5 cm of the sternoclavicular joint, and no patients complained of chronic donor-site pain or paresthesia. Thus, Nathe et al.’s study supports the safety and the efficacy of our method of minimizing the risk of nerve injury that can cause sensory disturbance around the incision. With respect to wound appearance, high levels of patient satisfaction were obtained with our method: most patients were highly satisfied with the cosmetic appearance of the donor-site operative scar. An additional advantage of our method is the ability to perform both ACDF and bone harvest in a single operative field, which can save the time and labor needed to prepare separate fields.
TABLE 5: Patient satisfaction with the cosmetic wound appearance* Degree of Satisfaction
No. of Patients (%)
very satisfied satisfied minor complaints dissatisfied
12 (86) 1 (7) 1 (7)† 0 (0)
* Data for 14 patients were available (response rate 88%). † The patient in Case 15 reported mild irregularity of the wound surface.
tal with a 6-month history of progressive movement disorder of his left arm and fingers and slight gait disturbance after undergoing ineffective conservative treatments at another clinic. His symptoms had caused him to quit his job as a taxi driver. Neurological examination revealed Grade 3/5 weakness in extension and flexion of his wrist and fingers and an elevated deep tendon reflex of both lower limbs. Neuroradiological examinations disclosed a C5–6 disc herniation with severe compression of the spinal cord and the left C-6 nerve root (Fig. 3A and B). The patient underwent ACDF with the method reported here. His symptoms gradually improved after postoperative rehabilitation, and he returned to his original job 4 months after the surgery. His MR images immediately after the surgery showed complete removal of the herniated disc and appropriate decompression of the spinal cord (Fig. 3C and D). Follow-up x-rays and CT scans (Fig. 4A–E)
Representative Case
A 48-year-old man (Case 14) presented to our hospi-
TABLE 4: Outcome by average VAS pain score* Time After Surgery
VAS Score (range)†
1 wk 1 mo 1 yr
1.1 (0–5) 0.8 (0–4) 0.1 (0–2)
* Score range: 0 = no pain, 10 = maximum pain imaginable. † Mean based on 14 patients whose data were available (response rate: 88%).
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Fig. 3. A and B: Preoperative T2-weighted MR images of the representative case showing a disc herniation at the C5–6 level, with severe compression of the spinal cord and the left C-6 nerve root. C and D: Postoperative images showing complete removal of the herniated disc and appropriate decompression of the spinal cord and left C-6 root, although high intensity in the central cord remains.
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Anterior cervical discectomy and fusion using clavicle bone
Fig. 4. Thin-section CT scans (A, C, and D) and 3D reconstruction images (B and E), and a skin photograph of a representative case (F), at 1 week (A–C) and 6 months (D–F) after the surgery. A: Sagittal image showing the position of an inserted cage at the C5–6 level. Note that the cleavage between the vertebral endplates and packed cancellous bone (arrows) is clearly visualized. B: 3D image demonstrating an inserted cage with faint metal artifact and a small rectangular bone window (asterisk) on the right clavicle. C: Axial image at the level of the right clavicle showing the radiolucent area (asterisk) under a small bone window indicating the bone defect after harvesting cancellous bone. D: Sagittal view revealing bone bridge formation (arrows) between both the endplates that has completely incorporated the cage. Note that the cleavage between the vertebral endplates and cancellous bone is obscure. E: 3D image showing that new bone formation (arrows) outside the cage has completely covered the surface of the cage and that healing of the donor site on the clavicle has also been completed. F: Photograph showing the appearance of the skin 6 months after surgery. There are 2 smooth and nearly unnoticeable surgical scars (arrows).
showed gradual development of bony fusion and spinal stability of the operated segment, finally resulting in rigid arthrodesis within 6 months after the surgery. Healing and cosmetic appearance of the both surgical wounds were uneventful, and the patient did not complain of pain or other morbidities at the donor site (Fig. 4F).
Conclusions
Compared with conventional ACDF using autologous iliac bone, our new method has the advantage of reducing donor-site morbidities; it also achieves a high level of patient satisfaction with the cosmetic appearance of the postoperative scars. Furthermore, high rates of bony fusion and cervical stabilization are achieved. To the best of our knowledge, this is the first report of the clinical use of clavicular bone for ACDF surgery. Acknowledgment We thank Norikazu Yamana, M.D., Department of Neurosurgery, Himeji Medical Center, Hyogo, Japan, for his kind assistance in data collection.
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Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Iwasaki. Acquisition of data: Iwasaki, Ikedo. Analysis and interpretation of data: Iwasaki, Hashikata. Drafting the article: Iwasaki. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Iwasaki. Study supervision: Iwasaki. References 1. Chau AM, Mobbs RJ: Bone graft substitutes in anterior cervical discectomy and fusion. Eur Spine J 18:449–464, 2009 2. Fowler BL, Dall BE, Rowe DE: Complications associated with harvesting autogenous iliac bone graft. Am J Orthop 24: 895–903, 1995 3. Heary RF, Schlenk RP, Sacchieri TA, Barone D, Brotea C: Persistent iliac crest donor site pain: independent outcome assessment. Neurosurgery 50:510–517, 2002 4. Hwang SL, Hwang YF, Lieu AS, Lin CL, Kuo TH, Su YF, et al: Outcome analyses of interbody titanium cage fusion used
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K. Iwasaki et al. in the anterior discectomy for cervical degenerative disc disease. J Spinal Disord Tech 18:326–331, 2005 5. Jagannathan J, Chankaew E, Urban P, Dumont AS, Sansur CA, Kern J, et al: Cosmetic and functional outcomes following paramedian and anterolateral retroperitoneal access in anterior lumbar spine surgery. Clinical article. J Neurosurg Spine 9:454–465, 2008 6. Jensen WK, Moore TA, Tribus CB, Anderson PA, Zdeblick TA: Use of patella allograft for anterior cervical diskectomy and fusion. J Spinal Disord Tech 22:392–398, 2009 7. Kurz LT, Garfin SR, Booth RE Jr: Harvesting autogenous iliac bone grafts. A review of complications and techniques. Spine (Phila Pa 1976) 14:1324–1331, 1989 8. Lebow R, Yao T, Stevenson CB, Cheng JS: Bone graft options, bone graft substitutes, and bone harvest techniques, in Winn HR (ed): Youmans Neurological Surgery, ed 6. Philadelphia: Elsevier, 2011, Vol 3, pp 2992–2998 9. Martin GJ Jr, Haid RW Jr, MacMillan M, Rodts GE Jr, Berkman R: Anterior cervical discectomy with freeze-dried fibula allograft. Overview of 317 cases and literature review. Spine (Phila Pa 1976) 24:852–859, 1999 10. Nathe T, Tseng S, Yoo B: The anatomy of the supraclavicular nerve during surgical approach to the clavicular shaft. Clin Orthop Relat Res 469:890–894, 2011 11. Odom GL, Finney W, Woodhall B: Cervical disk lesions. J Am Med Assoc 166:23–28, 1958 12. Pollock R, Alcelik I, Bhatia C, Chuter G, Lingutla K, Budithi C, et al: Donor site morbidity following iliac crest bone harvesting for cervical fusion: a comparison between minimally invasive and open techniques. Eur Spine J 17:845–852, 2008 13. Ryken TC, Heary RF, Matz PG, Anderson PA, Groff MW, Holly LT, et al: Techniques for cervical interbody grafting. J Neurosurg Spine 11:203–220, 2009
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14. Sangala JR, Nichols T, Uribe JS, Melton M, Vale FL: Sternal cancellous bone graft harvest for anterior cervical discectomy and fusion with interbody cage devices. Clin Neurol Neurosurg 112:470–473, 2010 15. Seiler JG III, Johnson J: Iliac crest autogenous bone grafting: donor site complications. J South Orthop Assoc 9:91–97, 2000 16. Shamsaldin M, Mouchaty H, Desogus N, Costagliola C, Di Lorenzo N: Evaluation of donor site pain after anterior iliac crest harvesting for cervical fusion: a prospective study on 50 patients. Acta Neurochir (Wien) 148:1071–1074, 2006 17. Skeppholm M, Olerud C: Pain from donor site after anterior cervical fusion with bone graft: a prospective randomized study with 12 months of follow-up. Eur Spine J 22:142–147, 2013 18. Smith GW, Robinson RA: The treatment of certain cervicalspine disorders by anterior removal of the intervertebral disc and interbody fusion. J Bone Joint Surg Am 40-A:607–624, 1958 19. Tubbs RS, Louis RG Jr, Wartmann CT, Cormier JL, Pearson BE, Loukas M, et al: Use of the clavicle in anterior cervical discectomy/corpectomy fusion procedures: cadaveric feasibility study. Childs Nerv Syst 24:337–341, 2008
Manuscript submitted November 5, 2013. Accepted July 21, 2014. Please include this information when citing this paper: published online August 29, 2014; DOI: 10.3171/2014.7.SPINE131000. Address correspondence to: Koichi Iwasaki, M.D., Department of Neurosurgery, Kitano Medical Research Institute and Hospital, 2-4-20 Ogi-machi, Kita-ku, Osaka 530-8480, Japan. email: todaiji [email protected].
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