From: "Douglas Smith, D.C." Date: Sun, 29 Dec 1996 11:08:42 -0800 Subject: Jrnl Article: Pathogenesis sports-related spondylolisthesis -------------- Enclosure number 1 ---------------- Citation: The American Journal of Sports Medicine, Jan-Feb 1996 v24 n1 Title: Pathogenesis of sports-related spondylolisthesis in adolescents: radiographic and magnetic resonance imaging study. Authors: Ikata, Takaaki; Miyake, Ryoji; Katoh, Shinsuke; Morita, Tetsuki; Murase, Masaaki Subjects: Spondylolisthesis_Development and progression Reference #: A17996885 ========================================== We reviewed radiographs and magnetic resonance images of 77 young athletes with spondylolysis and spondylolisthesis (more than 5% vertebral slip) (slip group). The results were compared with similar studies in 88 patients with spondylolysis only (nonslip group). Endplate lesions were found in all patients in the slip group and in 60 (68%) of those in the nonslip group. Slippage between the osseous and cartilaginous endplates was identified in the T1-weighted sagittal magnetic resonance images and categorized according to the type of slippage: total slip of L-5 or S-1, partial slip of L-5 or S-1, or a combination of these (mixed type). In a study of 31 patients whose slippages progressed, no slippage was associated with the early stage of a pars interarticularis defect. Most vertebral slippages developed or progressed in the cartilaginous or apophyseal stage of the lumbar skeletal age. Wedging of the L-5 vertebral body and rounding of the sacrum progressed as the slippage developed; these did not occur in the nonslip group. These results indicate that the advanced stage of a pars interarticularis defect in an immature spine is a risk factor for spondylolisthesis. The deformities of the lumbosacral spine are thought to be the secondary changes caused by vertebral slippage. ========================================= Spondylolisthesis is defined as the forward slipping of a vertebral body over the one below it. In spondylolisthesis (olisthesis) among athletes under the age of 18, the most commonly associated lesion is a defect of the pars interarticularis, which suggests there may be mechanical weakness in the neural arch.[5,12,21] Although spondylolysis is known to be a stress fracture of the pars interarticularis that is caused by repetitive athletic activities, the exact cause of vertebral slippage is still unknown.[2,4,8,9,11,13] Various factors that may cause slippage to advance have been discussed, including age, sex, initial degree of slippage, angle of slippage, low lumbar index, a rounded S-1, and lumbosacral spina bifida.[1,5,16,17,20,21] Vertebral slippage is said to progress more frequently during the rapid growth spurt in children, but Seitsalo et al.[17] reported that major slippage has already occurred by that time. Controversy exists as to the importance of L-5 wedging and rounding of the superior surface of S-1.[1,15,20] There is, however, no clear evidence as to what causes slippage to develop.[3] The purpose of this study was to clarify the pathogenesis of spondylolisthesis in young athletes with spondylolysis. Our explanation for this cause is based mainly on the magnetic resonance image (MRI) changes of signal intensity and morphology at the affected levels of the lumbosacral spine with an associated endplate lesion. METHODS We examined 77 young athletes (55 boys and 22 girls) with spondylolysis and spondylolisthesis (slip group) at our sports clinic during a 7-year period between 1987 and 1993. Spondylolisthesis was defined as more than 5% vertebral slippage. Patient ages ranged from 9 to 18 years (average, 14.0). Their skeletal ages based on the appearances of the secondary ossification center of L-3 were as follows: cartilaginous stage, 24 patients; apophyseal stage, 32 patients; and epiphyseal stage, 21 patients (Fig. 1). Pars defects showed a series of changes from the early to the terminal stage in radiographic findings.[11] These changes were characterized by an ill-circumscribed radiolucent defect in the early stage, a hairline defect occasionally accompanied by fragments in the progressive stage, and a wide defect with reactive sclerosis and hypertrophy in the terminal stage. Spondylolysis and spondylolisthesis were studied radiographically by AP, lateral, and oblique views of the lumbosacral area. The listhetic levels were all at L-5 to S-1. Wedging of the L-5 vertebral body and rounding of the upper endplate of S-1 were evaluated using the lumbar index and rounding index on plain lateral radiographs.[22] Magnetic resonance imaging studies were performed using a 0.5 T superconductive system (MRT-50A, Toshiba, Japan) with T1-weighted (repetition time, 500 msec; echo time, 30 msec) and T2-weighted (repetition time, 1600 msec; echo time, 100 msec) spin-echo sequences. Vertebral endplate lesions were classified according to the Tlweighted MRI scans as Grade 0 (normal), Grade 1 (concave, irregularity, or thinning), or Grade 2 (separation or detaching or both) (Fig. 2). Disk degeneration, recognized by changes in the signal intensity on T2-weighted MRI scans, was graded as 0 (normal), 1 (mild decrease), 2 (moderate decrease), and 3 (marked decrease). The results of the slip group were compared with those of similar studies in 88 young athletes (69 boys and 19 girls) with spondylolysis only (nonslip group). Their ages ranged from 7 to 18 years (average, 13.7). Skeletal ages assessed with the previous method were cartilaginous stage, 10 patients; apophyseal stage, 53 patients; and epiphyseal stage, 25 patients. All pars defects were detected at L-5. RESULTS The T1-weighted MRI scans demonstrated endplate lesions at the lower surface of L-5 or the upper surface of S-1 or both in all patients in the slip group and in 60 (68%) of the nonslip group. There was a Grade 2 lesion in all patients in the slip group and in 2 (2%) of the nonslip group. These differences were statistically significant Mann-Whitney U-test, P < 0.01) (Table 1). Endplate lesions in the slip group were accompanied by characteristic associated changes of slippage between the cartilaginous and osseous endplates. From the location of the endplate lesions, it was possible to identify five different types of slippage: a partial slip of L-5 or S-1, a total slip of L-5 or S-1, and a combination of these (mixed type). There was an incidence of 40%, 10%, 4%, 14%, and 32%, respectively (Fig. 3). Mean percent slippage was 15.7% in the patients with total slippage, 17.8% in those with a mixed type of slippage, and 11.2% in those with partial slippage. The degrees of percent slippage were significantly different between partial and total or mixed type (unpaired t-test, P < 0.05 for total slippage, P < 0.01 for mixed type). Disk degeneration was also seen in 39 (51%) of the slip group and in 17 (19%) of the nonslip group (Table 2). Ten patients (13%) in the slip group and one (1%) in the nonslip group had Grade 3 degeneration (marked decrease). These incidences were significantly different (Mann-whitney U-test, P < 0.01,). TABLE 1 Grade of Endplate Lesion Grade Group 0 1 2 No. (%) No. (%) No. (%) Slip (N = 77) 0 (0) 0 (0) 77 (100) Nonslip (N = 88) 28 (31.8) 58 (65.9) 2 (2.3) TABLE 2 Grade of Degeneration of the Intervertebral Disk Grade Group 0 1 2 3 Slip (N = 77) 37 (48.1) 20 (26.0) 9 (11.7) 10 (13.0) Nonslip (N = 88) 71 (80.7) 14 (15.9) 2 (2.3) 1 (1.1) Of 51 patients who were followed radiographically for more than 1 year, 22 showed an average slippage development of 9.8% (range, 6% to 14%) and 9 showed an average slippage progression of 13.1% (range, 6% to 33%) to 19.5% (range, 12% to 35%). The skeletal age of patients whose slippage developed and progressed were the cartilaginous stage in 16 patients, the apophyseal stage in 12 patients, and the epiphyseal stage in 3 patients. Twenty-two patients had slippages that developed or progressed in the progressive stage of pars defects, nine patients in the terminal stage, and none in the early stage. For those patients in the slip group who had development or progression of slippage, the lumbar index decreased significantly during the follow-up period, whereas wedging of the L-5 body in those patients in the nonslip group as well as those in the slip group who had no slippage progression remained unchanged (Fig. 4). During development or progression of slippage, rounding of the upper surface of the sacrum of patients in the slip group increased significantly during the follow-up period, whereas that of patients in the nonslip group and of patients in the slip group without slippage progression remained unchanged (Fig. 5). DISCUSSION Radiographic evidence of the progression of isthmic spondylolisthesis has been reported by numerous authors.[3,5,16,17] Seitsalo et al.,[17] in their long-term follow-up study of 272 patients with spondylolisthesis, found that 62 (23%) patients had more than 10% progression of spondylolisthesis. However, no clear cause of such progression has been determined. In the present study, the development and progression of spondylolisthesis were evaluated by MRI in 77 young athletes with spondylolisthesis following spondylolysis. The results showed that endplate lesions were more frequently observed at the lumbosacral spine with pars defects and vertebral slippage than with pars defects only. The incidence and MRI grading of endplate lesions tended to increase and progress with the increased degree of slippage and advanced stage of pars defect. We further identified and categorized slippage between cartilaginous and osseous endplates on MRI scans. The MRI scans revealed greater slippage in those cases where there was a total slip or a mixture of a total and a partial slip of L-5 or S-1. Therefore, it should be possible to predict from MRI scans whether slippage will progress. However, further study is necessary to understand whether partial slippage progresses to total or mixed slippage in slippage development. The stage of a pars defect could possibly contribute to slippage progression as we found that no slippage developed from a vertebra in the early stage of pars defect. Disk degeneration may also be a factor in slippage progression.[7,17,19] In the present series, disk degeneration was observed in both group of patients, but the degree of degeneration was not severe. These facts suggest that repetitive stress on the lumbosacral spine causes endplate lesions, such as nonarticular osteochondroses, as well as disk degeneration in association with pars defects.[6,10,11,18] However, because disk degeneration is still mild in young patients, the endplate lesion may contribute more to the development or progression of vertebral slippage. Controversy exists regarding other risk factors for the development or progression of slippage, including age, the low lumbar index of L-5, and the rounding of the superior surface of S-1.[1,5,20] Slippage progression occurs more frequently during the rapid growth period during adolescence.[5,17,19] Our results, using an evaluation system based on the skeletal age of the lumbar spine, also showed that a more matured spine has a lower risk of slippage development or progression. SUMMARY Our study showed that wedging of the L-5 body and rounding of the superior surface of S-1 increased in association with endplate lesions in young athletes with spondylolysis. This finding indicates that changes occurring in the caudal endplate of L-5 and in the cranial endplate of the sacrum should be considered as the consequence rather than the cause of the listhetic process. In conclusion, spondylolysis-associated endplate lesions at the lower edge of L-5 or the upper level of S-1, or both, in young athletes was found to have a high risk of slippage between the osseous and cartilaginous endplates, resulting in spondylolisthesis. The L-5 wedging and S-1 rounding alteration was recognized as sequelae of endplate lesions rather than the cause of spondylolisthesis. [Figures 1 to 5 ILLUSTRATION OMITTED] REFERENCES [1.] Boxall D, Bradford DS, Winter RB, et al: Management of severe spondylolisthesis in children and adolescents. J Bone Joint Surg 61A: 479-495, 1979 [2.] Cyron BM, Hutton WC: The fatigue strength of the lumbar neural arch in spondylolysis. J Bone Joint Surg 60B: 234-238, 1978 [3.] Danielson BI, Frennered AK, Irstam LKH: Radiologic progression of isthmic lumbar spondylolisthesis in young patients. Spine 16:422-425, 1991 [4.] Farfan HF, Osteria V, Lamy C: The mechanical etiology of spondylolysis and spondylolisthesis. Clin Orthop 117: 40-55, 1976 [5.] Fredrickson BE, Baker D, McHolick WJ, et al: The natural history of spondylolysis and spondylolisthesis. J Bone Joint Surg 66A: 699-707, 1984 [6.] Hickey DS, Hukins DWL: Relation between the structure of the annulus fibrosus and the function and failure of the intervertebral disc. Spine 5: 106-116, 1980 [7.] Hirabayashi K, Ikeda K, Tsuchihashi Z, et al: Spondylolysis and spondylolisthesis--pathological conditions and therapeutic indication. J Jpn Orthop Assoc 46: 675-694, 1972 [8.] Krenz J, Troup JDG: The structure of the pars interarticularis of the lower lumbar vertebrae and its relation to the etiology of spondylolysis. With a report of a healing fracture in the neural arch of a fourth lumbar vertebra. J Bone Joint Surg 55B: 735-741, 1973 [9.] Lafferty JF, Winter WG, Gambaro SA: Fatigue characteristics of posterior elements of vertebrae. J Bone Joint Surg 59A: 154-158, 1977 [10.] Macnab I: Anatomy, in Backache. Baltimore, Williams & Wilkins, 1977, pp 1-15 [11.] Morita T, Ikata T, Katoh S, et al: Lumbar spondylolysis in children and adolescents. J Bone Joint Surg 77B: 620-629, 1995 [12.] Newman PH: The etiology of spondylolisthesis. J Bone Joint Surg 45B: 39-59, 1963 [13.] O'Neill DB, Micheli LJ: Postoperative radiographic evidence for fatigue fracture as the etiology in spondylolysis. Spine 14: 1342-1355, 1989 [14.] Paajanen H, Tertti M: Association of incipient disc degeneration and instability in spondylolisthesis. A magnetic resonance and flexion-extension radiographic study of 20-year-old low back pain patients. Arch Orthop Trauma Surg 111: 16-19, 1991 [15.] Peterson CK, Haas M, Harger BL: A radiographic study of sacral base, sacrovertebral, and lumbosacral disc angles in persons with and without defects in the pars interarticularis. J Manipulative Physiol Ther 13: 491-497, 1990 [16.] Saraste H: Long-term clinical and radiological follow-up of spondylolysis and spondylolisthesis. J Pediat Orthop 7., 631-638, 1987 [17.] Seitsalo S, Osterman K, Hyvarinen H, et al: Progression of spondylolisthesis in children and adolescents. Spine 16: 417-421, 1991 [18.] Siffert RS: Classification of the osteochondroses. Clin Orthop 158:10-18, 1981 [19.] Szypryt EP, Twining P, Mulholland RC, et al: The prevalence of disc degeneration associated with neural arch defects of the lumbar spine assessed by magnetic resonance imaging. Spine 14: 977-981, 1989 [20.] Taillard W: Le spondylolisthesis chez l'enfant et l'adolescent. Acta Orthop Scand 24:115-144, 1954 [21.] Wiltse LL: The etiology of spondylolisthesis. J Bone Joint Surg 44A: 539-560, 1962 [22.] Wiltse LL, Winter RB: Terminology and measurement of spondylolisthesis. J Bone Joint Surg 65A: 768-772, 1983 Takaaki Ikata,([dagger]), MD, Ryoji Miyake, MD, Shinsuke Katoh, MD, Tetsuki Morita, MD, and Masaaki Murase, MD (*) Presented at the 20th annual meeting of the AOSSM, Palm Desert, California, June 1994. ([dagger] Address correspondence and reprint requests to Takaaki Ikata, MD, Professor and Director, the Department of Orthopedic Surgery, School of Medicine, the University of Tokushima, 3-18-15 Kuramoto-cho, Tokushima 770, Japan. No author or related institution has received any financial benefit from research in this study. ================================================