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A COMPARISON OF STRUCTURAL GRAFTS IN THE REPAIR OF LUMBAR PSEUDARTHROSIS: AUTOGENOUS ILIAC CREST VS. FEMORAL RING
ALLOGRAFT
DAVID B. COHEN, MD, MPH, AREESAK CHOTIVICHIT, MD,
TAKUYA FUJITA, MD, PHD,TZE-HONG WONG, MD
CAMERON B. HUCKELL, MD, ANN N. SIEBER, RN, MSN
JOHN P. KOSTUIK, MD, FRCS(C), H. CHRISTOPHER LAWSON, BSC
From Johns Hopkins University
School of Medicine Baltimore, Maryland (DBC, ANS, JPK, HCL) State University of New York at Buffalo Buffalo, New York (CBH) Faculty of Siriraj Hospital Mahidol University Bangkok,
Thailand (AC) Kanazawa University Kanazawa, Japan (TF) Taiwan Provincal Hsin-Chu Hospital Hsin-Chu City, Taiwan (T-HW)
Reprint requests to:
David B. Cohen, MD, MPH Department of Orthopaedic Surgery Johns
Hopkins University School of Medicine 601 North Caroline Street, Rm. 5235 Baltimore, MD 21287
Since Hibbs19 and Albee
1
first described their series of spinal fusions in 1911, various technical advances have occurred and new techniques have evolved that have led to the expansion of surgical indications for spinal fusions. With the advent of nonsegmental and segmental fixation, spinal fusions via anterior, posterior, or combined approaches have been performed to maintain spinal alignment,
35,38 correct mechanical instability, prevent neurologic injury and relieve pain.3,37,51
Among the indications for spinal fusion in revision spinal surgery, repair of pseudarthrosis represents one of the most common and most difficult problems to manage.4,11,13,26
Reported rates of
pseudarthrosis have varied in the literature depending upon the surgical indications, surgical techniques, patient factors (i.e., smoking), as well as the length and method of follow-up.26 In 1948, Cleveland
10 reported a pseudarthrosis rate of 20% following a posterior spinal fusion and rate of 10% following posterolateral fusion. Watkins49
reported a somewhat higher pseudarthrosis rate of 32% following posterolateral fusions. Macnab36
compared the pseudarthrosis rate following anterior fusions (30%), posterior fusions (17%) and inter-transverse fusion (7%). Stauffer and Frymoyer have reported a similar 20% rate of pseudarthrosis following posterolateral fusions.
16,44 In a recent review of the literature, Steinmann and Herkowitz reported that the incidence of pseudarthrosis varied from 0 to 68% depending upon the fusion technique used and the diseases being treated.
45
The use of instrumentation appears to affect the rate of pseudarthrosis in spinal fusion surgery. Brodsky et al. found that posterolateral. spinal fusions led to a 31.5% rate of pseudarthrosis
without the use of implants and a pseudarthrosis rate of only 13% with implants.6
Zdeblick reported similar results finding only 5% of pseudarthrosis with instrumentation compared to 35% without instrumentation.52
More recently, Fischgrund reported that the rate of pseudarthrosis following posterolateral fusion for degenerative spondylolisthesis was 18% for instrumented fusion and 55% for uninstrumented fusion.15
In order to repair spinal pseudarthrosis in salvage reconstruction situations, Crock et al. have advocated the use of an anterior interbody fusion with structural autogenous iliac crest bone grafts. 17
It was believed that the superior vascular supply of the anterior spine and the superior biornechanical environment in the anterior spinal column offers the optirnal environment for healing while having a low complication rate for an experienced surgeon.
2
However, this technique can only be used at a limited number of levels and is associated with a great deal of donor site morbidity. In 1994, Kozak et al. described another fusion technique of using a femoral ring allograft filled with autogenous morselized iliac crest graft as a structural support for an anterior interbody fusion. They demonstrated an excellent fusion rate of 97% (in primary cases) with minimal donor site morbidity.
28
The purpose of this study is to compare the fusion rate and clinical outcomes of pseudarthrosis repair in the lumbosacral spine using anterior interbody fusion with either structural autogenous
iliac crest grafts or femoral ring allografts.
MATERIALS AND METHODS
We retrospectively reviewed the records of all patients treated surgically for the diagnosis of pseudarthrosis during the period from
January 1991 through October 1994 by one surgeon (JPK) in our institution. Only patients treated with anterior interbody fusion and minimum 2-year follow-up for an initial diagnosis of pseudarthrosis following spinal
fusion for degenerative disease of lumbosacral spine were included. We identified 53 patients treated by two different techniques (group 1:33 patients treated with autogenous structural iliac crest bone grafts and group
11:20 patients treated with femoral ring allografts filled with morselized autograft). The only factor that determined the type of graft material utilized in each case was the date of surgery: iliac crest grafts were
used before June 1993 and allografts were used after that date. Another 21 patients (group III) treated during the same period of time with anterior fusion for the diagnosis of pseudarthrosis following spinal fusion for
scoliosis were identified as a control group for internal validity of patient-based outcomes measures.
In all cases a retroperitoneal approach to the lumbar spine was utilized. Either a left flank or left
paramedian incision was utilized depending upon the vertebral levels to be fused and the number of levels to be fused. Complete discectomies were performed at each level and vertebral cartilaginous endplates removed
back to bleeding bony endplates using bone chisels. In groups I and 111, structural iliac crest block grafts were used at the involved levels (Fig. 1). In group II, fresh frozen femoral shaft allografts; were cut to fit
in the disc space and packed with morselized autogenous bone taken from the inner table of the iliac crest (Fig. 2). At the L5-S 1 level, two titanium 6.5-mrn bone screws with 16-mm threads were inserted from the
superior end plate of L5 transfixing the bone grafts and purchasing in the sacrum placing compression across the grafts (Fig. 3). Fixation for the levels of L4-5 or above was accomplished using an ALPS (Advanced Spine
Technology, San Leandro, CA) anterolateral plate and bicortical locking screws.
Clinical follow-up was provided for all patients at minimal intervals of 6 weeks, 3 months, 6 months, I year, 18 months, 2 years,
and then yearly. Clinic charts of all patients were reviewed to assess demographic information and determine preoperative pain level (0 to 10), working status, and whether litigation was involved. A Modified
Greenough-Fraser Low Back Outcome Score's was used to determine functional outcome at follow-up. A telephone interview by a trained individual not involved in the patient's care was used to determine these factors at
final follow-up. All radiographs from the 6-month, 1 -year, 18-month, 2-year, and further follow-ups were reviewed by an independent spine surgeon not involved the care of these patients. In cases where allografts were
utilized, fusions were graded using the Bridwell and Lenke grading system for allograft incorporation into the host vertebrae.5
Statistical Analysis
All data from the patient records in this
study were entered into a personal computer and analyzed using STATA 5.0 (College Station, TX). For direct comparison of proportions, Chi-square analysis was utilized when larger numbers were in individual cells. Fisher
Exact analysis was performed with small or empty cell comparisons. For continuous data, two-tailed T-tests were utilized to compare group means.
TABLE 1. Summary of Patient Demographic Information
| |
Group I |
Group II |
Group III |
Number of patients |
33 |
20 |
21 |
Age (years) |
52.3 ± 3.2 |
52.5 ± 3.1 |
46.8 ± 2.9 |
Gender (M/F) |
15/18 |
8/12 |
3/18 |
Follow-up (months) |
60.8 ± 5.4 |
37.6 ± 4.3 |
57.8 ± 6.5 |
Number of prior surgeries |
3.3 ± 1.1 |
3.2 ± 1.1 |
1.7 ± 1.1 |
Smokers (%) |
10/33 (30%) |
5/20 (25%) |
7/21 (33%) |
Litigation (%) |
13/32(40%) |
7/18(38%) |
2/21 (10%) |
Number of levels repaired |
1.6 ± 0.7 |
1.9 ± 0.9 |
1.7± 0.8 |
RESULTS
Demographics
All patients in this study were drawn from the referral practice of
one spinal surgeon (JPK) in a tertiary academic center. General demographic information of the three groups of patients in this study is shown in Table 1. As would be expected, group III
(pseudarthrosis and scoliosis) did differ significantly from groups I and 11 (pseudarthrosis and degenerative disease) in several respects. Group III had significantly fewer patients involved in
litigation (p < 0.01), had a significantly higher proportion of women (p < 0.01), and was significantly younger (p < 0.05) than the other groups. When comparing groups I and II the only significant
difference between them was the average length of follow-up (p < 0.01), which is to be expected in any study of consecutive series. Otherwise, there were no significant differences between groups I and II.
Fusion
In group I (iliac crest grafts), 32 out of 33 patients (97%) went on to solid fusion with graft integration by 12-month follow-up with the
remaining patient going onto pseudarthrosis with hardware failure at 2-year follow-up. In group II [femoral ring allografts (FRA)], all 20 patients (100%) went on to fusion; however, clear radiographic
evidence of fusion took until the 2-year follow-up visit. At the 6 month follow-up, 24.3% of FRA patients had radiographic grade I appearance (fused and incorporated), 63.6% were grade 2 (partially
incorporated), and 12. 1 % were grade 3 (lucent line present); however, none were grade IV (pseudarthrosis with graft collapse). By 12 months, 81.6% of patients were grade 1, 18.4% were grade
2, and no patients were rated grade 3 or 4. At 18- and 24-month follow-ups all of the FRA patients were rated as grade 1. There was not a significant difference in the fusion rates between groups I and Il.
Outcomes
Functional outcomes were measured at final follow-up using the modified Greenough-Frazer Low Back Outcome Score (LBOS) scaled to a 100-point range. In group I, patients involved in litigation
averaged a significantly lower LBOS (p < 0.05) of 47 (range 35-55) than patients not involved in litigation [average LBOS 65 (range 56-77)]. When these groups were compared with our control group
III [average LBOS 67 (range 59-76)] we found that the litigation group were significantly worse (p < 0.05) in functional outcome, but no significant difference could be found with the non-litigation group.
Using a visual analog pain scale (VAS) to measure patient pain, we found that the patients in group I pain levels decreased from an average preoperative level of 8.3 to a final level of 5.5 at final
follow-up (p < 0.05). Similarly, in group 11, pain levels decreased from an average level of 8.2 to a final level of 5.5 at final follow-up (p < 0.05). However, there was no significant difference in the degree
of pain relief between the two treatment groups. Although none of the patients in either group I or H were able to work prior to surgery, 28% of patients in group 1 (3/13 litigation and 6/19 non-litigation
patients) and 36% of patients in group II (3/7 litigation and 4/11 non-litigation patients) were able to return to full employment.
Complications
None of the patients in any treatment group sustained major neurologic complications; however, one patient in the study had a hardware failure following autograft subsidence that resulted in an
iliac vein thrombosis at 18-month follow-up. Hardware removal and treatment with systemic anticoagulation for 3 months allowed the patient to go on to fusion without long-term vascular sequelae.
Three patients in group I and two patients in group II suffered from an ileus in the postoperative period. One patient in each group developed a postoperative pneumonia. One patient in group II
developed a screw backing out from the L3 vertebrae at 2-year follow-up despite a solid fusion.
DISCUSSION
Many studies looked at the fusion rates and clinical outcomes
following the repair of pseudarthrosis. The poor rates of successful fusion in pseudarthrosis repair seem to depend on numerous factors. The poor vascularity of the surgical/fusion bed2l and loss of
spinal alignment (flatback) 25,30 have both been indicated as reasons for the low success rates of pseudarthrosis repair via a posterior surgical approach. In 1988, Kostuik et al. demonstrated
that failure to restore sagittal plane balance and inadequate posterior bony surface area would lead to both return of deformity and pseudarthrosis.2,1 Additional mechanical factors such as
excessive stress shielding across the fusion site37 or insufficient internal/external stabilization33 have also been implicated in leading to pseudarthrosis. Other authors have pointed to numerous
metabolic factors such as osteoporosis, malnutrition, diabetes, osteomalacia,41 and nicotine usage42 as primary factors leading to pseudarthrosis. Boden42 and Brown7
have implicated theffects of tobacco use and anemia on local wound vascularity and oxygen delivery leading to poor fusion rates. Using a posterior approach with pedicle screw fixation, West et al. were able to obtain
successful fusion in only 11 of 17 patients (65%).50 Some other authors have achieved better results using a posterior approach in repairing simple hyper-trophic pseudarthrosis, but recommend a
combined anterior and posterior approach for more complex problems. 11,31,34,47
An anterior interbody fusion has been advocated by many authors
as a superior procedure for pseudarthrosis repair based upon the superior vascularity and mechanical environment for healing present in the anterior lumbar spine.26,34 Structilral iliac crest autograft has
been used for anterior graft material with rates of success ranging from 56%43 to up to 97%.17 However, structural iliac crest grafts
are not without their limitations. Due to the amount of available graft, donor site morbidity limits a surgeon to treat only one or two levels." Graft subsidence has also been found to be a significant
problem by several authors. Denis" found that 100% of grafts subsided with 46% having a final intervertebral height less than preoperative while Kozak2l found that 84% of grafts subsided an
average of 4 mm. Our current results in this study are consistent with these prior studies. We found that 97% of iliac crest graft patients went on to solid arthrodesis. In an attempt to prevent
subsidence, anterior hardware fixation was used in all cases. Despite these attempts, subsidence did occur in 35% of our iliac crest grafts but averaged only 2 mm. Our one major failure of
anterior fixation occurred in a patient who had an FRA placed at the L5-S I levels and iliac crest autografts at the L3-4 and L4-5 levels. Significant subsidence occurred at the autograft levels leading to a
tension failure of the proximal screws. Since we have started using an anterior plate with self-locking screws, we have not seen a problem with hardware failure.
In 1993, Kozak et al. described the use of femoral ring allografts filled with autogenous bone chips for primary spinal fusion.29 The use of femoral ring allografts filled with autogenous bone chips has
been gaining popularity for several reasons. The FRA provides a large contact area with the vertebral end plate surface for mechanical support and has a compressive strength at least seven
times greater than those forces seen in vivo.5,39 In addition, the use of FRAs allows the surgeon to treat multiple levels without subjecting the patient to as great an amount of donor site morbidity.8
Finally, the FRA can be technically easier to use than fibular allografts because a singular graft can be used at each level and one does not need to trough the FRAs into the vertebral bodies. 5,8,28,29
In the current study a great deal of care was taken in vertebral endplate preparation with chisels used to completely remove the cartilaginous end plate back to bleeding bone before
graft placement. Using these techniques and anterior instrumentation, we were able to obtain a 100% fusion rate with FRAs in cases of pseudarthrosis.
Obtaining a solid fusion has not necessarily resulted in good
restoration of function for patients with a diagnosis of pseudarthrosis.14,20,40.46,48 In 1990, Kozak had a fusion rate of 85% in repairing pseudarthrosis, but only 30% of his patients had
good clinical results.27 Kostuik et al. reported on 38 patients who underwent repair of pseudarthrosis with tricortical autogenous iliac crest grafts and obtained a 91% fusion rate, but only 43% of
patients returned to work.24 Of 68 patients treated by Carpenter with 51-month follow-up, 83% achieved a solid fusion with one surgery; however, 54% of patients had a poor result and only 28% returned to work.
9 Nearly 58% of patients in Carpenter's report were receiving workers' compensation preoperatively. Unfortunately, our results were not significantly different from those in the literature.
We were able to obtain 97% and 100% fusion rates in our two treatment groups; however, only 32% of our patients returned to work. In our patients, 40% were involved in active litigation at the
time of surgery, but there was no difference in the return to work rate between litigation and non-litigation patients.
It has been suggested that obtaining a solid fusion is important in
predicting a good outcome. In patients undergoing pseudarthrosis repair, Kim et al. found that 81% of patients who fused had satisfactory outcome while only 23% of patients who did not fuse had a satisfactory outcome.
22 In 1992, Lauerman was able to obtain a 49% fusion in 40 patients treated for pseudarthrosis.32 Overall, 86% of his patients had continued pain; however, 66% of
fused patients had a good or excellent result while only 14% of unfused patients had a similar result. On reviewing 46 patients who underwent pseudarthrosis repair, Kornblatt and Jacobs found that
85% of patients who fused improved clinically while 95% Of those who did not fuse failed to improve.23 In our current study we were unable to draw any conclusions about the effect of a solid fusion on
outcome. We had 52 of 53 patients go on to a solid fusion, so we did not have enough patients with a nonunion to perform any comparisons. The senior author has continued to use FRAs for the
anterior repair of pseudarthroses in additional patients. At a minimum 2-year follow-up, only two of the additional 52 patients have failed to heal with a continued pseudarthrosis rate of 4%.
The incorporation of different type of bone grafts can occur at different rates. Autograft bone often incorporates more rapidly than allografts in the same clinical and biological environment.8 Kozak
and Bridwell found that femoral ring allografts can take up to 2 years to incorporate fully.5,18 Although different criteria for fusion were used for our iliac crest and FRA groups, the assessment of
fusion was made using standard radiographs by the same observers. In our iliac crest group (group I), 97% of patients went on to clear fusion by 12-month follow-up (60% had clearly fused at 6
months). In our FRA group (group II), graft incorporation was graded according to Bridwell's criteria. All FRAs in this study did go on to fusion, but they took up to 18 months for the fusions to become
mature (grade 1). As an adjunct to the current study, the Bridwell Grading System was found to be less reliable than a simple assessment of fused vs. nonfused.
CONCLUSION
In this study, both structural autogenous iliac crest grafts or femoral ring allografts packed with autogenous chip graft were extremely effective in repairing pseudarthrosis when combined with
anterior internal fixation. We could not find a significant difference in either fusion rate or long-term functional outcomes between the two treatment groups. Given these findings, we believe that FRAs offer
advantages over iliac crest grafts in these difficult cases. Although FRAs took longer to demonstrate complete incorporation, we found less graft subsidence and loss of correction when FRAs were used.
We also found that more levels could be treated with an overall impression that there were fewer complaints associated with the donor graft site. However, a formal evaluation of complaints
associated with the donor site was not performed and should be more carefully evaluated in future studies. Additionally, we did find a difference in the time course of radiographic healing between the
two groups, but in the current study we did not look at the time course of functional recovery following surgery. Anecdotally, there did not appear to be a difference in recovery between the two
groups; however, further investigation is required to determine if one graft technique offers the patient a more rapid return of function or pain relief than another.
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