Double-level isthmic spondylolisthesis treated with posterior lumbar interbody fusion: A review of 32 cases

Double-level isthmic spondylolisthesis treated with posterior lumbar interbody fusion: A review of 32 cases

Clinical Neurology and Neurosurgery 161 (2017) 35–40 Contents lists available at ScienceDirect Clinical Neurology and Neurosurgery journal homepage:...

624KB Sizes 0 Downloads 67 Views

Clinical Neurology and Neurosurgery 161 (2017) 35–40

Contents lists available at ScienceDirect

Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro

Double-level isthmic spondylolisthesis treated with posterior lumbar interbody fusion: A review of 32 cases

MARK



DeYong Songa, DeWei Songb, KeHui Zhangc, Zhong Chend, , Feng Wange, TianHang Xuana a

Department of Spine Surgery, Foshan Hospital of Traditional Chinese Medicine, Foshan City, Guangdong Province, China Department of Minimally invasive pain treatment, Mengyin County Hospital, Linyi City, Shandong Province, China c Department of Neurosurgery, Foshan Hospital of Traditional Chinese Medicine, Foshan City, Guangdong Province, China d Department of Spine Surgery, Zhujiang Hospital of Southern Medical University, Guangzhou City, Guangdong Province, China e Department of Spine Surgery, Foshan Chancheng Central Hospital, Foshan City, Guangdong Province, China b

A R T I C L E I N F O

A B S T R A C T

Keywords: Double-level Spondylolisthesis Spinal fusion Outcomes

Objective: The incidence of double-level isthmic spondylolisthesis is rare. The aim of this study is to evaluate the short-term functional and radiological outcomes of surgical treatment for double-level isthmic spondylolisthesis. Patients and methods: Between 2004 and 2014, thirty-two patients with double-level isthmic spondylolisthesis who underwent posterior lumbar interbody fusion (PLIF) with autogenous bone chips were reviewed retrospectively. The clinical outcomes were measured by VAS (Visual analog scale) and JOA(Japanese Orthopedic Association) score. Results: At an average follow-up of 2.8 years, the mean score on the VAS of back pain and sciatica decreased from 6.48 and 4.26 points preoperatively to 1.82 and 1.10 points at final follow-up, respectively. The average JOA score improved from 13.8 ± 3.1 preoperative to 25.6 ± 1.3 (range, 17–28) points postoperative. The average recovery rate was 77.6%. The good and excellent rate was 84.3% (27/32). The fusion rate was 87.5% (28/32). Changes in disc height, degree of listhesis, whole lumbar lordosis, and sacral inclination between the pre- and postoperative periods were significant. Conclusions: Our findings suggest that PLIF with autogenous bone chips for double-level isthmic spondylolisthesis could yield good functional short-term results. It seems to be a viable approach in the treatment of double-level isthmic spondylolisthesis.

1. Introduction

2. Patients and methods

The term spondylolisthesis is defined as the forward displacement of the vertebra on its adjacent caudal vertebra. Isthmic spondylolisthesis is the most common type of spondylolisthesis in adults at approximately 4–6% of the general population [1,2]. Symptomatic patient with isthmic spondylolisthesis usually require surgical intervention. Multiple surgical procedures have been used to treat isthmic spondylolisthesis; However, the prevalence of double-level spondylolisthesis is rare and it is revealed in only a few cases [3–6]. The lack of large scale clinical trials on the management of this lesion make it difficult to define an optimal treatment algorithm. We are reporting on the clinical and radiological results of a series of double-level spondylolisthesis treated by PLIF with autogenous bone chips. To our knowledge, this is the largest series of double-level spondylolisthesis treated by this technique.

Between July 2004 and May 2014, 35 patients with double-level spondylolisthesis underwent PLIF with autogeneous bones were retrospectively reviewed in this study. The inclusion criteria for patients were the presence of double-level isthmic spondylolisthesis; persistent back pain with or without pain in the lower extremities pain who failed to respond to conservative treatment for at least 6 months; and no previous lumbar surgery or coexisting spinal deformity. Three patients who were lost to follow-up were excluded from this study. For the remaining 32 patients, the age of patients ranged from 36 to 67 years with the mean of 51.3 ± 10.25 years. There were 9 males (28.1%) and 23 females (71.8%). Main symptoms included low back pain in all cases, radiating leg pain in 25 (78.1%), numbness in 22(68.7%), weaknesses in 11 (34.3%), neurogenic claudication in 18(56.2%). The olisthetic level was at L4-5 and L5-S1 30 cases, at L3-4 and L4-5 2 cases. The minimum follow-up was 2-years (mean, 2.8 years; range, 24–72



Corresponding author at: No 253 Gong Ye Da Dao Zhong Road, Guangzhou City, Guangdong Province, China. E-mail address: [email protected] (Z. Chen).

http://dx.doi.org/10.1016/j.clineuro.2017.08.007 Received 20 May 2017; Received in revised form 11 August 2017; Accepted 15 August 2017 Available online 19 August 2017 0303-8467/ © 2017 Published by Elsevier B.V.

Clinical Neurology and Neurosurgery 161 (2017) 35–40

D. Song et al.

of the anterior, middle, and posterior intervertebral disc heights by three [7]. The amount of slippage was quantified according to the classification proposed by Meyerding [8].The angles of whole lumbar lordosis, pelvic incidence, and sacral inclination were recorded to evaluate sagittal alignment (Fig. 1). Radiologic proof of solid fusion required fulfillment of the following criteria: no radiolucent gap at the vertebral endplate interface, no evidence of mobility in flexion-extension roentgenogram, and presence of bridging trabeculae across the area of arthrodesis.

Table 1 Demographics. N = 32 Average age

51.3 ± 10.25

Male Female

9 23

28.1% 71.8%

Main symptoms Low back pain Radiating leg pain Neurogenic claudication Numbness Weakness

32 25 18 22 11

100% 78.1% 56.2% 68.7% 34.3%

Olisthetic Levels L4-5 and L5-S1 L3-4 and L4-5

30 2

93.7% 6.2%

3. Surgical technique The patients were carefully positioned in the prone position under general anesthesia. A routine midline approach was made. Reduction and regular pedicle screws were inserted in the conventional technique. Decompression was commenced via the midline. After central decompression, the foramina were inspected and decompressed nerves were then retracted medially to expose the disc space. A ring incision was made on one side of the annulus and the disc material was removed with pituitary rongeurs. After removal of the disc, the rods were contoured and cut to length after templating. Both rods were applied to the pedicle screw heads, with nut application. Then the disc space was distracted and reduction was performed from bottom to top, the lower vertebra was used as a fulcrum. The endplates of the vertebrae were denuded by scrapers, without weakening the subchondral bone plates. In all cases, the bone procured from the decompression was cleared of any soft tissue and preserved to perform the bony fusion. Chips were compressed into the disc space to make it compact using a variety of straight and curved bone tamps. A keystone plug was tapped in posterior to the bone fragments and locked into place (The plug was made of large piece of lamina acquired during decompression). The plug was then countersunk approximately 2–5 mm to prevent iatrogenic compression of the cauda equina. A visual check ensured that there was no nerve root compression following the insertion of chips. Final tightening of the nuts was performed under compression with the torque wrench.

Table 2 The change in the pre- operation and final follow-up JOA scores. Preoperative

Final follow-up

Recovery rate

13.8 ± 3.1

25.6 ± 1.3

77.6%

months). The summary of patient data is tabulated in Table 1. The clinical outcomes were based on the visual analogue scale (VAS) for the preoperative back pain and radiating pain at the 1st, 6th, 12th and 24th postoperative month. Functional outcomes were measured using Japanese Orthopedic Association score (JOA score) preoperatively and at the last follow-up [Table 2]. The recovery rate of JOA score was calculated according to the formula: the recovery rate = [(postoperative score-preoperative score)/(29-pre-operative score)] × 100%. Excellent > = 75%, Good 50–74%, Fair 25–49%, Poor 0–24%. Radiographic evaluation includes anteroposterior and lateral plain radiographs at each post-operative visit as well as flexion/extension lateral radiographs at one and two years post-operatively. The intervertebral height was calculated at the lateral X-ray by dividing the sum

Fig. 1. All parameters were measured on standing upright lateral radiographs of the spine (a) ce/cd, slipping percentage; LL whole lumbar lordosis (b) (a + b + c/3) intervertebral height (c) PI, pelvic incidence; SS, sacral slope (sacral inclination).

36

Clinical Neurology and Neurosurgery 161 (2017) 35–40

D. Song et al.

Fig. 2. Comparison between pre-and post-operative VAS.

55.3°,56°,33.2°respectively; they were changed to 47.5°,55°, and 41°at the last follow-up. The change of whole lumbar lordosis and sacral inclination demonstrated statistical differences (P < 0.001) (Table 3). Procedure-related complications included two malpositioned screws, which necessitated intraoperative repositioning. One patient had superficial wound infection, which was treated successfully by drainage and antibiotics. Screws loosening and pullout were present in one patient, the patient then underwent revision surgery, with extension of the instrumented fusion to the above veterbra.

Table 3 Pre-and post-operative radiological data. Parameter

Pro-OP

Post-OP

P value

Degree of listhesis(%) L3-4 level L4-5 level L5-S1 level

7.4 ± 2.3 19.1 ± 10.2 8.5 ± 5.4

3.2 ± 2.6 3.6 ± 4.8 2.9 ± 2.4

< 0.001 < 0.001 < 0.001

Intervertebral disc height(mm) L3-4 level L4-5 level L5-S1 level Whole lumbar lordosis Pelvic incidence Sacral inclination

6.9 ± 3.1 7.5 ± 5.7 9.2 ± 2.3 55.3 ± 9.8° 56 ± 11.4° 33.2 ± 4.8°

7.08 ± 1.2 11.6 ± 2.1 12.4 ± 1.9 47.5 ± 9.2 55 ± 9.68° 41 ± 6.8°

n/s < 0.001 < 0.001 < 0.001 n/s < 0.001

5. Discussion Multiple-level spondylolytic defects of the spine is rare. Based on reported incidences at the time, Ravichandran calculated that only 1.48% of patients with back pain were diagnosed with multi-level spondylolysis [9]. It is not surprising that the prevalence of multiplelevel spondylolisthesis is even rarer. The exact etiology and predisposing factors for progression of the slip to spondylolisthesis remain uncertain. It has been shown that isthmic spondylolisthesis has a multifactorial origin: genetic factor, trauma, mechanical, and hormonal factors are all believed to play a role [10,11,5]. The majority of patients in this study are manual worker, but none of them have major trauma. Therefore, their lesions were probably caused by repetitive stress and congenital predisposition. Kalichman L et al. reported that the incidence of isthmic spondylolisthesis is higher in males [12]. However, in the current series of double-level isthmic spondylolisthesis, we observed that the incidence in females is nearly three times than that of males. These findings seemed consistent with the report that females are more likely to suffer progression of spondylolisthesis[13].Many studies have shown that 24–70% patients of isthmic spondylolisthesis are associated with spina bifida occulta [14–16]. In this study,a spina bifida occulta was found in only 3 patients. All of the spina bifida occulta were at S1 level, which is different from the report that a spina bifida occulta was usually present at the same level with pars defect [17]. In spite of the most common site of isthmic spondylolisthesis is at the L5-S1 level. In this study, we found that degree of listhesis at L5-S1 was less than that of L4-L5 level. Although numerous techniques have been used to treat isthmic spondylolisthesis, instrumented fusion of the subluxated segments is the most common procedure. Our surgical strategy consists of decompression of the spinal canal and nerve roots, as well as reduction and fusion utilizing PLIF with autogeneous bone chips. We preferred this

3.1. Statistical analysis A t-test was performed to establish if the difference between the preoperative and postoperative value of the main parameters was significant. A probability value of less than 0.05 was considered significant. 4. Results The mean score on the VAS of back pain improved from 6.48 points preoperatively to 3.46 points at one month postoperative and decreased to 2.36, 2.28, and 1.82 at postoperative 6, 12 and 24 months respectively. The VAS of sciatica fell from 4.26 at preoperative to 2.32 at one month postoperatively, and it reduced to 1.70, 1.28, and 1.10 at 6, 12 and 24 months postoperative, respectively (Fig. 2). The preoperative average JOA score was 13.8 ± 3.1(range, 3–17) points. At final follow-up, the average JOA score improved to 25.6 ± 1.3 (range, 17–28) points. The average recovery rate was 77.6% (Table 2).The good and excellent rate was 84.3% (27/32). The main radiological results are given in Table 3. Of the 32 cases, solid union was observed in 28 cases (87.5%) (Figs. 3, 4). The mean intervertebral disc height of L4-5 level and L5-S1level increased from 7.5 to 11.6 and 9.2–12.4 mm (p < 0.001) respectively at last followup. The mean degree of listhesis (%)at L3-4,L4-5 and L5-S1 were 7.4%,19.1% and 8.5% respectively; they were changed to 3.2%,3,6% and 2.9% (P < 0.001) at last follow-up. The mean preoperative angles of whole lumbar lordosis, pelvic incidence, and sacral inclination were 37

Clinical Neurology and Neurosurgery 161 (2017) 35–40

D. Song et al.

Fig. 3. Anteroposterior (a) and lateral (b) preoperative radiographs revealing pars defects at L4 and L5 and double-level spondylolisthesis both grade I at L4/L5 and at L5/S1. Computed tomography axial scan demonstrating defect bilaterally at the L-4 (c) and L-5 (d) in the pars. Magnetic resonance imaging (MRI) revealed degenerative disc disease at L4-5 and L5-S1, hypertrophic ligamentum flavum at L4-L5 (e). Lateral (f) postoperative radiographs showing reduction was preserved, and fusion was achieved.

VAS, reflected a substantial clinical improvement in our cases. The radiological results also demonstrated that there were significant changes of slip percentage and disc height between preoperative and postoperative assessments. The question whether the reduction of the slippage is necessary remains a topic of debate.The literatures have shown no significant difference between the results of fusion with or without associated reduction for single-level low-grade subluxation [20–22]. On the other hand, other authors demonstrated the advantages of reduction [23–25]. They insisted that, theoretically, it not

procedure because it offers several advantages. It can completely decompress the nerve roots, and discectomy is crucial to eliminate discogenic back pain [18]. It could provide a wider area of intervertebral bone-to-graft contact area than posterolateral fusion. In addition, and it also can increase load sharing of the grafts because 80% of the weight bearing is supported by anterior and middle spinal columns [19]. Furthermore, pedicle screw devices could exert immediate mechanical support after restoration of sagittal alignment. The clinical and functional outcomes, assessed by the JOA score and 38

Clinical Neurology and Neurosurgery 161 (2017) 35–40

D. Song et al.

Fig. 4. Anteroposterior (a) and lateral (b) preoperative radiographs showing pars defects at L4 and L5 and double-level spondylolisthesis both grade II at L4/L5 and at L5/S1. MRI revealed degenerative disc disease at L4-5 and L5-S1 (c)). Computed tomography axial scan revealing pars defect bilaterally at the L-4 (d) and L-5 (e) Lateral (f) postoperative radiographs showing reduction of spondylolisthesis, restoration of the disc height and solid interbody fusion.

muscle, which is a major cause of prolonged lower back pain following surgery [26]; and high fusion rate. Recently transforaminal interbody fusion (TLIF) has been frequently used to manage isthmic spondylolisthesis [27–29]. This technique allows exiting and transvering roots to be decompressed simultaneously, with the benefit of less destruction of the posterior column of the spine. In theory, it also can prevent typical complications of anterior and posterior lumbar interbody fusion. A combination of anterior and posterior approaches has also been recommended [30–32]. This technique can thoroughly decompress the nerves, increase fusion rate and improve correction of the deformity [33,34]. However, those approaches have not been documented for the treatment of double-level isthmic spondylolisthesis. Whether or not those techniques are suitable for double-level spondylolisthesis should be further studied. Some authors recommend preoperative pars block for detecting of the source of pain and defining the appropriate operative procedure [35–37]. They concluded that this technique is safe and reliable in predicting a successful outcome for patients with spondylolysis and

only can restore physiological lumbar balance, but also improve the fusion success by reducing the shearing force. In addition, the reduction/distraction procedure allows for restoration of the neural foraminal area. Given our reported results, it can be concluded that anatomic reduction and fusion has improved clinical and radiological results.The fusion rate was 87.5% at the final follow-up. The result was comparable with other series using this technique for treating lumbar spondylolisthesis [25]. Results of the present study indicate that there was a significant difference with regard to lumbar lordosis and sacral inclination following surgery. Those findings also suggest that sagittal imbalance due to double-level isthmic spondylolisthesis may be corrected by reduction and fusion of the slipped levels. The alternative technique to achieve similar objectives would be anterior lumbar interbody fusion (ALIF).This technique can indirectly decompress the nerve root through a widening of the intervertebral space with several advantages: avoiding the epidural scarring, which may effect the long-term clinical outcomes of posterior surgery; avoidance denervation due to extensive stripping of the paraspinal 39

Clinical Neurology and Neurosurgery 161 (2017) 35–40

D. Song et al.

history, Semin. Spine Surg. 1 (1989) 78–94. [17] B.E. Fredrickson, D. Baker, W.J. McHolick, H.A. Yuan, J.P. Lubicky, The natural history of spondylolysis and spondylolisthesis, J. Bone Joint Surg. Am. 66 (1984) 699–707. [18] C.R. Weatherley, C.F. Prickett, J.P. O‘Brien, Discogenic pain persisting despite solid posterior fusion, J. Bone Joint Surg. Br. 68 (1986) 142–143. [19] K.H. Yang, A.I. King, Mechanism of facet load transmission as a hypothesis for lowback pain, Spine (Phaila Pa 1976) 9 (1984) 557–565. [20] L.L. Wiltse, D.W. Jackson, Treatment of spondylolisthesis and spondylolysis in children, Clin. Orthop. Relat. Res. 117 (1976) 92–100. [21] M. Muschik, H. Zippel, C. Perka, Surgical management of severe sopndylolisthesis in children and adolescent. Anterior fusion in situ versus anterior spondylodesis with posterior transpedicular instrumentation and reduction, Spine (Phila Pa 1976) 22 (1997) 2036–2042. [22] J.P. Ghosez, O. Himmer, B. Devyver, R. Rossillon, A. Beuqnies, L. Lootvoet, Surgical treatment of isthemic spondylolisthesis. A comparative study of 3 types of arthrodesis, Rev. Chir. Orthop. Reparatrice Appar. Mot. 78 (1992) 515–528. [23] J. Swan, E. Hurwitz, F. Malek, E. van den Haak, I. Cheng, T. Alamin, E. Carragee, Surgical treatment for unstable low-grade isthmic spondylolisthesis in adults: a prospective controlled study of posterior instrumented fusion compared with combined anterior-posterior fusion, Spine J. 6 (2006) 606–614. [24] E.N. Hanley Jr., Decompression and distraction-derotation arthrodesis for degenerative spondylolisthesis, Spine (Phila Pa 1976) 11 (1986) 269–276. [25] G. La Rosa, A. Conti, F. Cacciola, S. Cardali, D. La Torre, N.M. Gambadauro, F. Tomasello, Pedicle screw fixation for isthmic spondylolisthesis: does posterior lumbar interbody fusion improve outcome over posterolateral fusion, J. Neurosurg. 99 (2003) 143–150. [26] L. Hackenberg, H. Halm, V. Bullmann, V. Vieth, M. Schneider, U. Liljenqvist, Transforaminal lumbar interbody fusion: a safe technique with satisfactory three to five year results, Eur. Spine 4 (2005) 551–558. [27] C.A. Chastain, J.C. Eck, S.D. Hodges, S.C. Humphreys, P. Levi, Transforaminal lumbar interbody fusion: a retrospective study of long-term pain relief and fusion outcomes, Orthopedics 30 (2007) 389–392. [28] S. Lauber, T.L. Schulte, U. Liljenqvist, H. Halm, L. Hackenberg, Clinical and radiologic 2-4-year results of transforaminal lumbar interbody fusion in degenerative and isthmic spondylolisthesis grades1 and 2, Spine (Phila Pa 1976) 31 (2006) 1693–1698. [29] J.K. Houten, N.H. Post, J.W. Dryer, T.J. Errico, Clinical and radiographically/ neuroimaging documented outcome in transforaminal lumbar interbody fusion, Neurosurg. Focus 20 (2006) E8. [30] J. Swan, E. Hurwitz, F. Malek, van den Haak, I. Cheng, T. Alamin, E. Carragee, Surgical treatment for unstable low-grade isthmic spondylolisthesis in adults:a prospective controlled study of posterior instrumented fusion compared with combined anterior-posterior fusion, Spine J. 6 (2006) 606–614. [31] B.K. Kwon, A.S. Hilibrand, K. Malloy, P.E. Savas, M.T. Silva, T.J. Albert, A.R. Vaccaro, A critical analysis of the literature regarding surgical approach and outcome for adult low-grade isthmic spondylolisthesis, J. Spinal Disord. Tech. (2005) S30–S40. [32] T.S. Videbaek, F.B. Christensen, R. Soegaard, E.S. Hansen, K. Høy, P. Helmig, et al., Circumferential fusion improves outcome in comparison with instrumented posterolateral fusion: long-term results of a randomized clinical trial, Spine(Phila Pa 1976) 31 (2006) 2875–2880. [33] M. Spruit, P.W. Pavlov, J. Leitao, M. De Kleuver, P.G. Anderson, F. Den Boer, Posterior reduction and anterior lumbar interbody fusion in symptomatic low-grade adult isthmic spondylolisthesis: short-term radiological and functional outcome, Eur. Spine J. 1 (2002) 428–433. [34] D.S. Bradford, O. Boachie-Adjei, Treatment of severe spondylolistheses by anterior and posterior reduction and stabilization, J. Bone Joint Surg. Am. 72 (1990) 1060–1066. [35] P.B. Suh, S.I. Esses, J.P. Kostuik, Repair of pars interarticularis defect. The prognostic value of infiltration, Spine (Phila Pa 1976) 16 (1991) S445–448. [36] S. Vidyadhara, Rationale in the management of 4-level lumbar spondylolyses with or without instability and/or spondylolisthesis, Spine (Phila Pa 1976) 39 (12) (2014) E734–E738. [37] D.S. Bradford, J. Iza, Repair of the defect in spondylolysis and minimal degrees of spondylolisthesis by segmental wire fixation and bone grafting, Spine (Phila Pa 1976) 10 (1985) 673–679.

low-grade spondylolisthesis. We did not use this method, because, as to our knowledge, the predictive value has not been demonstrated for the treatment of double-level spondylolisthesis. In addition, considering the anatomical structure disorganization is more complicated than that of spondylolyisis. Its diagnostic value for double-level spondylolisthesis needs to be further verified. There are some limitations in the present study. Firstly, it was a retrospective with a short follow-up period; Secondly, a CT scan was not used for assessing fusion status because of expense and radiation protection. Thin slice CT scan and sagittal reconstructions would improve the accuracy of fusion status. 6. Conclusion The incidence of double-level isthmic spondylolisthesis is rare. Our treatment approach proved successful in this study. We therefore think that in treating double-level spondylolisthesis, a combination of decompression, anatomic reduction, and PLIF with autogenous bone chips seems to be a viable approach. Acknowledgement None. References [1] C.J. Standaert, S.A. Herring, Spondylolysis: a critical review, Br. J. Sports Med. 34 (2000) 415–422. [2] H. Moller, R. Hedlund, Instrumented and non-instrumented posterolateral fusion in adult spondylolisthesis-a prospective randomized study:part 2, Spine (Phila Pa 1976) 25 (2000) 1716–1721. [3] M. Da Silva, Spondylolisthesis; report on a case with double spondylolisthesis, J. Belge Radiol. 35 (1952) 284–303. [4] A. Walch, Spondylolisthesis. 2 cases of double spondylolisthesis, Acta Orthop. Belg. 23 (1957) 252–255. [5] L.C. Wong, Rehabilitation of a patient with a rare multi-level isthmic spondylolisthesis: a case report, J. Can. Chiropr. Assoc. 48 (2004) 142–151. [6] D. Song, Z. Chen, D. Song, Surgical treatment of double-level isthmic spondylolisthesis, J. Neurosurg. Spine 20 (2014) 396–399. [7] W. Frobin, P. Brinckmann, M. Biggemann, Objective measurement of the height of lumbar intervertebral disc from lateral roentgen views of the spine, Z. Orthop. Ihre Grenzgeb. 135 (1997) 394–402. [8] H.W. Meyerding, Spondylolisthesis, Surg. Gynecol. Obstet. 54 (1932) 371–377. [9] G. Ravichandran, Multiple lumbar spondylolyses, Spine (Phila Pa 1976) 5 (1980) 552–557. [10] M. Albanese, P.D. Pizzutillo, Family study of spondylolysis and spondylolisthesis, J. Pediatr. Orthop. 2 (1982) 496–499. [11] H. Ogawa, H. Nishimoto, H. Hosoe, N. Suzuki, Y. Kanamori, K. Shimizu, Clinical outcome after segmental wire fixation and bone grafting for repair of the defects in multiple level lumbar spondylolysis, J. Spinal Disord. Tech. 20 (2007) 521–525. [12] L. Kalichman, D.H. Kim, L. Li, A. Guermazi, V. Berkin, D.J. Hunter, Spondylolysis and spondylolisthesis: prevalence and association with low back pain in the adult community-based population, Spine (Phila Pa 1976) 34 (2009) 199–205. [13] A. Ganju, Isthmic spondylolisthesis, Neurosurg. Focus 13 (1) (2002) E1. [14] H. Saraste, The etiology of spondylolysis. A retrospective radiographic study, Acta Orthop. Scand. 56 (1985) 253–255. [15] P.H. Newman, Degenerative spondylolisthesis, Orthop. Clin. North Am. 6 (1975) 197–198. [16] L.L. Wiltse, L.G. Rothman, Sopndylolisthesis:classification,diagnosis,and natural

40