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Anterior cervical fusion with stand-alone trabecular metal cages (porous tantalum) for the surgical treatment of cervical myelopathy caused by degenerative disc disease. Preliminary observations in a series of 88 consecutive cases with minimum 12-month follow-up.





Authors: 
Luciano Mastronardi, MD, PhD � Raffaelino Roperto, MD - Guglielmo Cacciotti, MD �Alessandro Rinaldi, MD � Francesco Calvosa, MD 

Affiliation:
Department of Neurosurgery, San Filippo Neri Hospital - ASL Roma 1, Roma, Italy




Running head: ACF with trabecular metal cages 


Key Words: anterior cervical fusion � anterior cervical discectomy � cervical myelopathy trabecular metal cages � porus tantalum



Corresponding Author: Luciano Mastronardi, M.D., Ph.D., Via Reno 14, 00198, Roma, Italy � phone: ++390633062318 - fax: ++390633062284 � e-mail: mastronardinch@gmail.com


Abstract: STUDY DESIGN: Retrospective analysis of 88 consecutive patients with one-level or two-level degenerative disc disease producing cervical myelopathy treated by interbody fusion with stand alone trabecular metal (TM) cages. OBJECTIVE: To determine the safety and efficiency of stand alone TM (or porous tantalum) cages for anterior cervical fusion (ACF). SUMMARY OF BACKGROUND DATA: ACF with autologous bone has been reported over 50 years ago. The continuous development of materials with elastic modulus close to that of the cortical bone improves induction of osteogenesis and simplifies the technique of interbody fusion. The main purposes of bone substitutes for ACF are immediate biomechanical support, osteointegration of the graft, and elimination of donor site local side effects. This report shows our results using TM cages for the treatment of cervical myelopathy caused by one-level or two-level degenerative disc disease. MATERIALS AND METHODS: During a 65-month period, 88 consecutive patients had cervical fusions at 105 levels between C3 and C7. All surgeries involved one or two intervertebral spaces for degenerative disc disease producing mild or severe cervical spine myelopathy, in 31 patients (35,2%) associated to unilateral or bilateral radiculopathy. We implanted all disc spaces with unfilled TM trapezoidal cages (Zimmer Biomet Spine, Broomfield, CO). RESULTS: At a mean follow-up of 31 months (minimum 12, maximum 65) 95,4% of patients had a good to excellent outcome, with subjective and objective improvement of myelopathy; the result was fair in two and poor in other two patients. Radicular pain and/or deficit disappeared in 84 cases (95,4%) complaining preoperative mielo-radiculopathy. The cervical interbody fusion rate was 68.2% at 6 months and 100% at one year. Device fragmentation was never observed. In 2 cases, a second operation with removal of TM cages, corpectomy, expansion cages, and plating was necessary, after 3 and 8 months, respectively. CONCLUSIONS: TM cages appear to be safe and efficient for ACF in myelopathic patients. In order to confirm our preliminary impressions studies on larger series with long-term follow-up are warranted.

INTRODUCTION
Anterior cervical microdiscectomy is usually performed for degenerative disease that produces osteophytes and/or herniated disk provoking radiculopathy and/or myelopathy. Surgical intervention is indicated after the failure of an adequate period of conservative treatment1,2. When spinal cord compression for degenerative cervical spine disease at one or more disc level causes myelopathy with or without brachialgia, anterior cervical microdiscectomy and osteophytectomy followed by arthrodesis and fusion are almost worldwide accepted standard procedures, even if several Authors sustain that fusion procedure following anterior cervical discectomy is not absolutely necessary3,4,5,6 . Interbody bone grafting or cages, with or without anterior plating, are considered the gold-standard treatment for the surgical treatment of cervical myelopathy due to segmental degenerative disc disease.
The goals of bone substitutes for ACF are: biomechanical support, to restore foraminal height, to shore up cervical lordosis, to guarantee optimal osteointegration, and to reduce donor site complication, with shorter hospital stay7,8,9,10,11,12. During the last two decades standalone cages of various materials, which allow immediate stability without plates and screws, have been developed.
The ideal cage for ACF should ensure immediate structural support and subsequent adequate osteointegration and stability. A determining factor is the capacity of a given material to be elastically deformed by external forces, returning to its initial shape or position once the load is removed13,14. This capacity is the so called elastic modulus (EM): higher EM require higher forces for deforming temporarily the material. Among several metals, the TM (porous tantalum) is an open-cell porous biomaterial with a structure similar to trabecular bone. The structure of porous tantalum affords a high volumetric porosity, a low EM, and relatively high frictional characteristics15,16,17. Moreover, TM is extremely inert and resistant to acid corrosion18. All these characteristics make tantalum ideal for orthopedic implants17 and, therefore, an excellent biomaterial for ACF cages.
On the basis of these considerations, we investigated the bony incorporation of TM cages inserted in the interspace after anterior cervical spine microdiscectomy and osteophytectomy. With the aim to determine the affordability of this device, outcomes, fusion rates, and complications were assessed in 88 consecutive patients with a minimum follow-up of 12 months operated on for segmental degenerative cervical disc disease producing one-level or two-level spondylotic myelopathy.

MATERIAL AND METHODS

Patient Population
From July 2010 to December 2015, a consecutive series of 88 patients participated in the study.
Thirtyseven were males and 51 females, with an average age of 58.8 years (median: 59; range 44-83 years). Only patients requiring one-level or two-level surgery at contiguous disk spaces between C3-C4 and C6-C7 for a degenerative disk disease were considered eligible. Patients with multisegmental cervical stenosis, 3-level disk compressions, diffuse and severe arthrosis, previous treated level, traumatic herniation, and poor general health conditions were disqualified from the study. In order to ensure a homogeneous group of patients, biomechanical differences were considered between simple discectomy and corpectomy procedures, in regard to cervical alignment and translational movement of the strut affecting the clinical and radiological outcome. For this study, therefore, we selected only patients with cervical myelopathy caused by spinal cord compression at the level of one or two discs, which was treatable with microdiscectomy, osteophytectomy, arthrodesis, and subsequent fusion by anterior approach. Patients with more extensive cord compression necessitating corpectomy and fixation have been excluded. 

Fortyseven patients (53.4%) had a smoking history. Presenting symptoms included mild to severe myelopathic symptoms on inferior limbs only in 19 patients (21.6%) or in the four limbs in 69 (78.4%), associated to radiculopathy in 23 cases (26.1%.) The mean preoperative Nurick grade was 1.4�0.5.
Preoperative diagnosis was performed by means MRI in all cases: it showed various grade of alteration of the intramedullary signal in 79 cases (89.8%). In 21 of them, both hypointensity on T1-weighted images and hyperintensity on T2-weighted images were observed, whereas in 58 cases, only hyperintensity on T2-weighted imaging was present. 

Surgical Procedure
Single-level (71 cases) and two-level (17 cases) procedures accounted for 105 inserted implants. Under general anesthesia, a microsurgical anterior approach with the Smith-Robinson technique (modified according to Caspar) was performed. With adequate distraction, the vertebral endplates were symmetrically drilled; complete discectomy and osteophytectomy was obtained. In all cases, adequate exposure and decompression of dura and origin of nerve roots was obtained. The single-level or two-level arthrodesis for ACF was performed with TM trapezoidal cages of various sizes (Zimmer Biomet Spine, Broomfield, CO). The cage is a trapezoidal-shaped and slightly wedged implant made from trabecular metal (porous tantalum), an open-cell porous biomaterial having a structure similar to human trabecular cancellous bone. 
Before the closure of superficial layers, an intraoperative lateral fluoroscopic control was done and the correct position of the implant was checked: in 3 cases it was necessary to replace the implant in a better position. After the operation, all patients wore a soft cervical collar during the first 3-4 weeks.

Outcome measures 
Clinic and radiographic controls (including standard and flexion-extension radiographs) were conducted at periodic intervals after surgery: 1st post-operative day, 1 week (only clinic evaluation), 3 months, 6 months, and 12 months after surgery. Cervical x-rays were reviewed by an independent radiologist: the fusion was considered complete when: a) trabecular bone across the interfaces and trabecular bridging bone formation at the anterior and/or posterior surface of involved vertebral bodies appeared (the so called �sentinel signs�), b) lucencies between cage and vertebral plates disappeared, c) less than 5 degrees of flexion-extension range of motion a the fusion site, and d) disc height preserved, without collapse-induced kyphosis19. 
The level of patients� satisfaction was assessed by two questions at each clinical visit: I) are the symptoms the same, better or worse after surgery? and II) are you satisfied with the results of surgical treatment? Following hospital discharge, patients were also asked to record: 1) requirement of postoperative analgesics (monitored by the patient response yes/no to the daily question: Have you used the pain medication prescribed to you to relieve the pain for which you underwent surgery?) and 2) postoperative work-time loss (number of days lost from work after surgery). 

RESULTS
Mean operative time was 75 minutes (range 55-80) for one-level and 93 minutes (range 75-105) for two-level procedures. Postoperative mortality was zero and overall rate of complications 5.7%. In particular, worsening of myelopathy associated to fixation failure occurred in two patients (2.3%), worsening of myelopathy without fixation failure in other two (2.3%), and superficial wound infection in one case (1.1%), the last resolved with antibiotics and daily medications in outpatient basis.
Overall hospital stay after operation averaged 1.43 days (range 1-3) with a low requirement of analgesics. In particular, during the first 48 post-operative hours, 7 patients (7.9%) still complained slight neck and radicular pain, requiring oral or parenteral analgesics. We never observed permanent hoarseness or swallowing complaints; transient hoarseness was referred by 4 patients (4,5%: from 4 to 7 weeks) and transient swallowing was observed in other 4 (4,5%: from 3 to 24 days).
Implant related complications requiring a further surgical treatment were observed in 2 patients (2.3%), who had a failure of fixation and needed a second operation for late worsening of myelopathy after a first period of improvement: both cases were treated with removal of TM cages, corpectomy, expansion cages, and plating, 3 and 8 months after the first operation, respectively. 
Follow-up evaluation data greater than or equal to 12 months were available for all patients. At a mean clinical follow-up of 35.8 months (median 37; range 12-65) radicular and neck pain disappeared in all cases and patients� perception of outcomes was generally good (15 cases, 17%) or excellent (69 cases, 78.4%). The result was referred as �good� only from those patients who experienced transient post-operative complications and from patients who still complained slight pain during the first post-operative days. Four patients without any improvement or with slight worsening of myelopathic complain considered their result as fair. Very good clinical results have also been obtained in smokers. All working-active patients return to work within 4-6 weeks, especially if activities were not too heavy and the preoperative myelopathy not too severe. 
Cervical x-rays examinations performed during the follow-up period never showed breaking, collapsing, angular deformation, subsidence, pseudoarthrosis, fragmentation or protruding at the level of the TM cages, except for the 2 patients reoperated on for failure of the implant. In particular, in the first case, a 68-year-old man with a severe C5-C6 and C6-C7 preoperative myelopathy, we observed a small fracture of inferior vertebral endplate of C6 and bone fragment dislocation (with new �osteophyte-like� compression) 15 days after discharge. In the second patient, a posterior dislocation of TM cage occurred after a mild head-cervical trauma 8 months after surgery. Signs of pathological re-absorption and necrosis were not found in the contiguous vertebral bodies and inflammatory reactions were never seen aroud cages. In 9 cases a slight or moderate kyphosis was observed at the 3-month x-ray control, was improved at the 6-month control and was not completely disappeared at 12-month follow-up. 
Fusion was observed after 3 months in 17 out 41 non-smoker patients (41.5%) and in 2 out of 47 smokers (4.2%); the overall fusion rate at 3 months was 21.6%. Six months after surgery fusion was detected in 36 non-smokers (87.8%) and in 23 smokers (48.9%), respectively; the overal fusion rate at 6 months was 68.2%. After 12 months the fusion rate was 100% in both groups. 
During this period of follow-up, we did not observe any case with clinical and MRI features of degeneration changes of adjacent disc levels. 

DISCUSSION 
Cervical myelopathy caused by degenerative verterbal disease at one or more disc level is the most common cause of spinal dysfunction and non-traumatic spastic paraparesis and quadri-paresis in the elderly20. It is a chronic devastating disease that may be improved by surgical decompression and fusion in many patients, while in a minority the surgical treatment do not change neurological condition or the natural course of the diseases. Factors affecting prognosis and results of decompressive surgeries for myelopathy caused by degenerative cervical spine disease were discussed by many authors21,22,23. The most important affecting factors documented seems to be; age, duration of symptoms, preoperative transverse diameter of the spinal cord at the site of maximal compression, and signal intensity changes on pre-operative MRI21,24,25,26,27,28,29,30.
Intramedullary spinal cord changes of signal in spondylotic myelopathy can be reversible (hyperintensity on T2wi) or not-reversible (hypointensity on T1wi)

. The regression of the hyperintensity on T2wi is associated with a better prognosis, whereas the T1 hypointensity is not reversible; therefore, in these cases the prognosis is usually worse20,22,26,27,28,29,30,31,32. 
There are not enough information regarding the possible different outcome in relation to the early or late regression of T2-hyperintensity. Anyway, our preliminary experience seemed to exclude a relationship between time of signal recovery, the amount of re-expansion of the spinal cord at the level of maximal compression, and long-term outcome of cervical myelopathy26.
During the last two decades the use of bone autograft is gradually decreased, mainly because of the high rate of local side effects (pain, hematoma, scarring, infection, visible iliac crest defect). It has been supplied by allografts and, mainly, by several types of interbody spacers (cages) made of synthetic materials8,9,10,11,12,19,33,34,35, with or without anterior plating36. Even if the mean fusion time is shorter with bone autograft, the current implants used for arthrodesis and fusion allow an immediate biomechanical support, restore the height of disc space and intervertebral foramina, restrict mobility, and prevent collapse of the disc space reducing the incidence of subsequent kyphotic deformity8,10,11,12,19. This structural support and the subsequent successful osteointegration and fusion allow the re-absorption of residual osteophytes. This consideration justifies the lesser invasive surgical approach, both in terms of interspace drilling and consequently in terms of cage dimension.
The ideal device for ACF following anterior cervical discectomy has yet not been identified and seems to be in relation to several variables (age, quality of bone, pre-existing adjacent disease)37,38. In a previous article, we investigated the bony incorporation of a composite implant made by carbon fiber cage containing coralline hydroxylapatite, demonstrating a very low complication rate and a good fusion rate and clinical outcome38. In a second paper37 we reported our retrospective analysis of 36 cases of degenerative disc disease treated by interbody fusion with polyetheretherketone (PEEK) cages. About 97% of patients had a good outcome and the cervical fusion rate was 61.1% at 6 months and 100% at one year. PEEK cages appeared to be safe and efficient for ACF and the result was fair in only one myelopathic patient37. Even if this and other composite implants seem to ensure good or excellent results8,10,11,12,19,37,38,39, in the selection of cages an increasing relevance has the concept of �elastic modulus� (EM), that is the capacity of a material to be elastically deformed by an external force, returning to its initial shape or position removing the load13,14. A lower EM results in a more natural compatibility with respect to bone material. This concept is strictly connected to the possible accelerated degeneration of adjacent disc levels due to increased stress induced by fusion40,41,42,43,44,45,46,47,48,49,50,51. Symptomatic adjacent-segment disease occurrs at a mean incidence of 2.9% per year (range 0-4.8%) during the ten years after ACF with autogenous bone graft, especially at the C5-C6 and C6-C7 interspaces (p<0.0001)47. Therefore, 25.6% of patients who had an ACF with autogenous bone graft would have new disease at an adjacent level within ten years after surgery and about 70% of them need additional operative procedures47. The lower is the EM the lower seems to be the stress induced by ACF, the lower should be the adjacent-level disease41,48,49, and the higher the bony growth in and around the cage52. Therefore, in order to approximate the rate of adjacent-level disease to that one observed with autogenous bone graft47, the biomateral used for realizing cages for ACF should have an EM close to the bone. 
Experimental studies demonstrated that the EM of TM corresponds to that one of a mixture of bone obtained from human subchondral and cancellous bone13,53, leading to better load transfer and minimizing the stress-shielding phenomenon. Also for these reasons TM cages appear highly suitable for ACF after cervical microdiscectomy53,54,55,56,57. 
Porous tantalum or Trabecular Metal, is an open-cell porous biomaterial with a structure similar to human trabecular cancellous bone by having three-dimensional dodecahedron repeats. It has an average porosity of up to 80% with a consistent, open pore structure designed to resemble the physical and mechanical properties of cancellous bone. The coefficient of friction of TM cages is one of the highest among biomaterials, allowing for sufficient primary stabilization of implants53. Different fusion rates and results have been achieved in anterior cervical fusion using porous tantalum cages, which lead to contradictory views among spine surgeons53,54,55,56,57,58,59. Even if in the lumbar spine, trabecular metal has been demonstrated to be effective in obtaining fusion and improving patient outcomes after anterior as well as posterior lumbar interbody fusion53, in a prospective, randomized, controlled study on 80 consecutive patients, L�fgren et al59 reported that TM showed a statistically significant lower single-level ACF rate than the group treated with tricortical autograft (69% versus 92%, respectively). In accordance with them, Kasliwal et al58 concluded their prospective, randomized clinical study on 39 patients treated for a single-level degenerative cervical disk disease considering porous tantalum not ideal for ACF. Anyway, the number of cases enrolled in every single arm of the study is quite low for any statistical validation58.
In contrast with these two papers, many other Authors reported very encouraging results using TM cages for ACF in degenerative disk disease. More than 10 years ago, Vicario et al57 reported good clinical and radiological results by using tantalum cages in a preliminary series of 24 consecutive patients. In 2012, Fern�ndez-Fairen et al56 evaluated in a series of 61 cases (28 treated with TM cages) if ACF with porus tantalum implants can be considered a cost-effective method to treat cervical disk degenerative disease with radiculopathy. The Authors concluded that this device can be safely used as a stand-alone cage and is less costly and more effective compared to bone autograft with plating56. Recently, in the international literature there was a reappraisal of this argument, with several papers confirming the effectiveness of TM cages for ACF in degenerative spinal disease53,54,55. On a consecutive series of 99 patients with a mean follow-up of more than 5 years, Papacci et al55 reported a long term statistically significant clinical good results and a low rate of complications. At the same time, King et al54 reported their preliminary experience on fusion 6, 12, and 24 month post-operatively in a series of 10 cases treated by using TM cages in anterior cervical corpectomy, reporting 100% fusion rate and a low rate of subsidence 2 years after surgery.
On the basis of this literature analysis, we report the largest series (88 cases and 105 implants) of ACF performed with porus tantalum (or TM) cages, on a selected series of myelopathic patients, with or without radiculopathy. Treating myelopathic patients with degeneratice disk disease by means ACF with TM cages, we obtained encouraging preliminary results. In particular, our overall rate of complications was quite low (5.7%): worsening of myelopathy associated to failure of the implant occurred in two patients and worsening of myelopathy without fixation failure in other two. At a mean follow-up of 35.8 months patients� perception of clinical outcome was referred as good (17%) or excellent (78.4%). Four patients without improvement or with slight worsening of myelopathy considered their result as fair. In particular, 2 out 4 patients have been reoperated on: in the first, a small fracture of inferior vertebral endplate of C6 and bone fragment dislocation created after some weeks a new �osteophyte-like� compression; in the second, a posterior dislocation of TM cage after a mild head-cervical trauma occurred 8 months after surgery. 
As regard radiological results, overall fusion was observed after 3 months in 21,6% of patients: 41.5% non-smokers and in 4,2% smokers. Six months after surgery fusion was obtained in 87.8% of non-smokers and in 48.9% of smokers and the overall fusion rate was 68.2%. After 12 months the fusion rate was 100% in both groups. A slight or moderate kyphosis was observed in 9 cases at 3-month x-ray control, improved at 6-month control but not disappeared after 12-month; we did not observe any case with clinical and MRI features of degeneration changes of adjacent disc levels. 

CONCLUSIONS
In conclusion, our preliminary observations suggest that porous tantalum (TM) cages can be considered excellent bone substitutes for ACF after anterior cervical microdiscectomy and osteophytectomy at one or two level for the treatment of patients with cervical spondylotic myelopathy. In our series, TM stand-alone cages ensured a good fusion rate, with low-rate complications. In order to confirm our encouraging results and the possible role of porous tantalum in reducing the incidence of symptomatic adjacent-segment disease, studies on larger series are warranted.

DISCLOSURE
The Authors have no financial interest in the products or methodology advanced in this manuscript.


ABBREVIATIONS


TM = trabecular metal (tantalum)
ACF = anterior cervical fusion
EM = elastic modulus
MRI = magnetic resonance imaging
T1wi and T2wi = T1 and T2 weighted images
PEEK = polyetheretherketone

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