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Anatomy/Pathogenesis

New Concepts on the Pathogenesis and Classification of Spondylolisthesis

Hammerberg, Kim W., MD

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doi: 10.1097/01.brs.0000155576.62159.1c
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Spondylolisthesis is an easily recognized deformity, yet confusion persists over its natural history and preferred treatment. Some spondylolistheses progress to severe deformity resulting in moderate pain and neurologic compromise. Other slips progress very little and but produce significant symptoms. Sometimes, spondylolisthesis is only discovered incidentally. Why does this apparent paradox exist? Thirty years ago, Dandy and Shannon recognized that confusion arose from the mistaken belief that all spondylolistheses must have a single cause.1 It should now be understood that each type of spondylolisthesis is the similar radiographic end result of different and distinct disease processes. These disparate pathologic conditions produce spondylolisthesis because of the common morphology and biomechanical forces applied to the lumbosacral junction.

Morphology

The lumbosacral joint is the keystone of the axial skeleton. Its function is to provide stability by supporting physiologic loads, preventing nonphysiologic motion, and protecting the neural elements.

The spine can be conceptualized as a two-column structure. The anterior column of vertebral bodies and discs progressively enlarges in size and mass from cranial to caudal. The L5 vertebral body is the largest and is somewhat trapezoidal in shape in the sagittal profile. The sacrum provides a bony shelf to support the proximal spinal column. The orientation of the sacrum is interdependent on pelvic rotation, hip extension, and overall lordosis.2 The normal sacral inclination is between 40° and 60°. The intersegmental angulation between L5 and S1 is lordotic, and the lumbosacral angle ranges from −20° to −30°.3–5 The relationship between L5 and S1 is, in part, maintained by the intervening intervertebral disc. At this level, the disc is usually 10 to 15 mm in height, with a surface area of approximately 30 × 50 mm.6 The anulus fibrosus is composed of obliquely oriented fibers in concentric laminated bands.

The configuration of the lumbosacral anatomy in spondylolisthesis can be variable as demonstrated by Antonaides et al.7 The same forces that cause spondylolisthesis may also produce deformities of the sacrum in growing children. The relationships between sacral slope, pelvic inclination, and lumbar lordosis are dependent on the pelvic incidence. The pelvic incidence is unique to each individual and is the only fixed pelvic or spinal parameter. It increases with age but stabilizes after puberty, usually averaging 53° (range, 34°–77°).8 A high pelvic incidence results in high shear forces at the lumbosacral junction. Studies by Hanson et al10 and others2,9,11 have confirmed observations that spondylolisthesis is usually associated with a pelvic incidence greater than the mean and that a higher degree of slippage is associated with a higher pelvic incidence.

The posterior column is composed of bony and ligamentous structures. The bony elements include the zygapophysial joints, pars interarticularis, laminae, spinous processes, and transverse processes. The lumbosacral articulations are oriented at a 45° angle to the coronal and sagittal planes. The laterally situated superior facets of S1 are concave, and the medially situated inferior facets of L5 are convex. The lumbosacral facets are invested in a synovial lined capsule reinforced by insertions of the ligamentous structures.

The lamina, spinous process, and transverse process provide attachment for the erector spinae musculature as well as the posterior ligaments. The pars interarticularis acts as a bolt uniting the superior and inferior facets. The pedicle acts as a bridge between the anterior and posterior columns.

In static equipoise, stability of the spine requires very little muscular activity. Stability is rendered by the overall coronal and sagittal balance of the spinal column and the integrity of the osteo-discal-ligamentous complex. At the lumbosacral junction, stability is dependent on the spatial orientation of L5 to the sacrum, lumbosacral angle, sacral slope, and pelvic incidence as well as an intact osteo-discal-ligamentous complex. Because spinal parameters are dependent on pelvic parameters, alterations in local spatial orientation, such as spondylolisthesis, can produce global spinal imbalance (Figure 1).

Figure 1
Figure 1:
A, a high dysplastic developmental spondylolisthesis represents a true lumbosacral kyphosis and produces marked global sagittal imbalance of the thoracolumbar spine. B, the reduction of the monosegmental pathology results in marked improvement in sagittal balance.

Stability during dynamic function, in other words, with motion or load bearing, is dependent on the neuromuscular system as well as the osteo-distal-ligamentous complex. Motion is permitted through the disc because of its viscoelastic properties. Motion is passively restricted by the ligaments and posterior facets. Total combined flexion-extension at L5–S1 ranges from 14° to 20°.12–15 This is greater than the upper lumbar levels. Axial rotation ranges from 1.3° to 5°, the least of the lumbar spine. Lateral bending ranges from 1.5° to 5.5°.

Biomechanics

Nachemson et al have shown that the contents of the nucleus pulposus are strongly hydrophilic with a resting internal hydrostatic pressure of 1.5 kg/cm2.16 The compressive loads on the lumbar disc in vivo under physiologic loads has been found to exceed 2,000 N.16,17 The ultimate strength of a lumbar motion unit is between 4,000 N and 10,000 N.18–20

The high loads experienced by the lumbosacral spine are well documented, but how are these loads distributed? Loads applied to the lumbosacral spine are usually shared between the disc and posterior articulations, hence the concept of load sharing.21 Cyron et al.22 and Troup23 presented a simplified two-dimensional analysis of the forces acting at the lumbosacral disc in the erect posture. Their analysis indicates that compression is resisted by the disc. Shear is resisted by both the disc, and the posterior elements in concert with the action of the sacrospinalis and multifidus muscles.24,25

Cadaver studies by Adams and Hutton show that the apophyseal joints resist 16% of intervertebral compressive forces in lordotic postures but resist very little in the flexed postures.26 These findings are similar to those of other investigators who suggest the facets carry 12% to 25% of the combined loads.27–29 The distribution of loads shared by the posterior elements and intervertebral disc varies with posture and the individual morphology of the trijoint complex.16,17,30

When an intact functional spinal unit is loaded, the facet joints resist the majority of the shear force, while the disc is primarily subjected to compression. If the facets are ablated, the disc will readily creep forward secondary to stress relaxation.31 Haher et al have identified an alternate path of loading of the lumbar spine.32 Ablation of the posterior facets led to transfer of axial loads to the anulus and anterior longitudinal ligaments. They concluded that the load transfer could conceivably accelerate disc degeneration.

Resistance to torsion depends primarily on the integrity of the facet joints, whereas resistance to lateral bending is dependent on the integrity of the disc and perhaps the iliolumbar ligaments.33 Resistance to flexion is primarily dependent on the capsular ligaments of the facet joints. The disc, supraspinous and intraspinous ligaments, and the ligamentum flavum constitute secondary restraints.31

The lumbosacral facet joints protect the intervertebral disc from excessive shear, flexion, and axial rotation. Clearly, when the posterior bony elements are dissociated from the anterior column, the disc experiences unusually high shear forces, which can lead to spondylolisthesis. The importance of the posterior bony hook acting as a tension band to protect the anterior column is reflected in its strength. Troup25 and Cyron and Hutton34 found that the strength of the L5 isthmus was in the order of 2,000 N. Lamy et al found the force for failure was about 50% higher or proportionally close to that of a femur.35

The mechanism of failure of a normal pars interarticularis is through a fatigue fracture. Stewart, from his observations of Eskimos, felt that repetitive flexion was responsible for the fractures.36 Lamy et al similarly implicated flexion.35 Jayson37 and Shah et al38 found the site of maximal strain under central compression loads was on the superficial and deep surfaces of the pars interarticularis. Under posterior offset loads simulating extension, the compressive and tensile strains were increased at the isthmus. Their findings suggest that hyperextension leads to spondylolysis.

Studies by Cyron et al22 and Cyron and Hutton34 suggest that alternate loading may be responsible for the development of pars interarticularis fatigue fractures. More recently, Green et al have demonstrated large stress reversals in cadaver pars secondary to alternate flexion and extension loading.39 They agree that alternate loading is the most likely etiology for the development of spondylolysis.

These findings corroborate clinical observations that people involved in repetitious alternate loading activities such as gymnastics, weight lifting, and football have higher incidences of spondylolysis. Cyron and Hutton suggest that young people are more likely to develop spondylolysis because they engage in more strenuous activity and that their discs retain sufficient viscoelasticity to accommodate the significant reversals in motion that are necessary to lead to a fatigue fracture.34

Classification

Marchetti and Bartolozzi have developed an etiology-based classification system that differentiates between the various pathologic processes leading to spondylolisthesis.40 Two main categories of spondylolisthesis are defined (Table 1). One primary category is identified by primary developmental deficiencies at the lumbosacral junction resulting in various degrees of dysplasia. The other main category, acquired spondylolisthesis, is a result of traumatic, iatrogenic, pathologic, or degenerative causes.

Table 1
Table 1:
Marchetti-Bartolozzi Classification of Spondylolisthesis

The term “isthmic” should be avoided because it is a nonspecific anatomic reference and does not differentiate between developmental and acquired forms of spondylolisthesis. Both types may have defects of the pars interarticularis, but they represent significantly different pathologic processes.

Developmental spondylolisthesis is analogous to developmental dysplasia of the hip, which can progress to a frank dislocation depending on the degree of dysplasia and other factors such as age, growth, weight bearing, and muscle imbalance. In developmental spondylolisthesis, posterior deficiencies in the bony hook, that is, in the lamina, pars interarticularis, and lumbosacral facets may predispose to slippage. In addition, inadequacies of the anterior column including the intervertebral disc, body of L5, and sacral shelf may increase the likelihood of slippage. In the growing child, bony remodeling as a result of adaptation to the altered biomechanical forces may contribute to the development of high-grade slippage. A major component of the progression observed in high dysplastic slips may be due to growth abnormalities.

The developmental forms of spondylolisthesis are further subdivided into high dysplastic and low dysplastic types. The high dysplastic form is usually at L5–S1 and becomes symptomatic in adolescents. Radiographically, they are characterized by a wedge L5 and a domed and vertical sacrum. The anterior translation of L5 is associated with angulation producing a true lumbosacral kyphosis. These slips have the potential to develop into spondyloptosis if untreated or mismanaged (Figure 2).

Figure 2
Figure 2:
A and B, radiographs demonstrating the typical features of a high-grade dysplastic spondylolisthesis. The frontal view shows dysplastic posterior elements including spina bifida and hypoplastic inferior facets. The lateral view demonstrates a trapezoidal L5, domed and vertical sacrum, and attenuated and fractured pars interarticularis.

In the past, this type has been described as congenital, but it is not congenital in the true sense of the word as it is not present at birth. True congenital spondylolisthesis has been reported by Bradford et al as lumbosacral kyphosis.41 However, it is extremely rare, and like teratologic hip dislocation, is usually part of a more inclusive syndrome.

Patients with the low dysplastic forms of developmental spondylolisthesis usually present as young adults. Spina bifida occulta is frequently observed. The slippage is characterized by translation without the angulatory or kyphotic component. However, a patient at age 5 years with a low dysplastic form may, by the age 15 years, have a high dysplastic form secondary to growth, remodeling, and adaptive changes.

Many clinical and radiographic factors have been analyzed as predictors of slip progression. These include female gender, prepubescence, increased slip angle, trapezoidal L5, domed and vertical sacrum, and sagittal rotation.42 It is difficult to determine if these parameters are primary or secondary adaptive changes. Ikata et al proposed that L5 wedging and S1 doming are actually adaptive changes.43

Increasing evidence suggests that growth, or more specifically abnormal growth, is the most powerful influence on slip progression. Ikata et al observed that slippage occurred between the osseous and cartilaginous endplates during the apophyseal stage of lumbar skeletal grown.43 Takahashi et al reviewed the MRI scans of 13 patients with severe spondylolisthesis.44 They found a unique defect of the anterosuperior shelf of the sacrum, which appeared during progression and led to lumbosacral kyphosis. They termed the resulting deformity kyphospondylolisthesis, a high-grade slip. Investigations by Kajiura et al confirmed the role of a biomechanical weakness in the vertebral growth plate as an important mechanism in spondylolisthesis.45

An impairment of the vertebral growth plate as the basic lesion in producing slippage in immature spines was also demonstrated by Sakamaki et al.46 Pars defects were created in immature and mature rat spines. Slippage was observed in the immature rats but not in the adult rats. Histologic examinations showed growth plate injury in the immature rat apophyses and disc degeneration in the mature rat spines. These findings suggest that developmental spondylolisthesis may be the sacral equivalent of Blount’s disease of the tibia (Figure 3).

Figure 3
Figure 3:
A, an anteroposterior tomogram of an adolescent’s knee with severe Blount’s disease. Fragmentation of the medial epiphysis is evident as well as a marked angular deformity of the medial tibial metaphysis. B, a sagittal CT scan of an adolescent’s lumbosacral spine with high dysplastic spondylolisthesis. There is fragmentation of the anterosuperior endplate of the sacrum and a deformity of the sacral shelf very similar to that of the tibia. Is dysplastic spondylolisthesis the equivalent of Blount’s disease of the sacrum?

The degree of developmental dysplasia at the lumbosacral junction and the growth potential of the patient are the most important predictors of progression. The presence or absence of an isthmic defect is noted, but of secondary significance. Indeed, high-grade forms of developmental spondylolisthesis with intact posterior elements demand special caution. This situation may arise by elongation of the posterior elements secondary to repeated microfractures and subsequent healing as the disc bond slowly fails allowing ventral translation. These slips present a high risk of neurologic compromise, including cauda equina syndrome before or during surgical intervention (Figure 4).47

Figure 4
Figure 4:
A and B, T1 and T2 sagittal MRI of a patient with low dysplastic developmental spondylolisthesis with intact posterior elements and a cauda equina syndrome. The slippage results in a high-grade stenosis as the cauda equina is pinched between the lamina and bulging disc at the lumbosacral junction.

The acquired forms of spondylolisthesis include traumatic, postsurgical, pathologic, and degenerative etiologies. Traumatic spondylolisthesis can be the result of a single high-energy injury and is probably better considered as a fracture dislocation. The other type of acquired traumatic spondylolisthesis is secondary to stress or fatigue fracture through a normal pars interarticularis, termed spondylolytic in this discussion. Spondylolytic spondylolisthesis usually presents in young to middle-aged adults as low back pain. This injury is being seen more frequently in younger patients as emphasis on organized sports has increased. The morphology of the lumbar spine and sacrum is normal (Figure 5). The stress fracture is usually at L5 but may be higher and, in some cases, at multiple levels.48 A fracture observed through dysplastic posterior elements, as in spina bifida, is regarded as a developmental rather than an acquired spondylolisthesis. Frequently, a history of an activity requiring repetitive lumbar flexion and extension is elicited. Initially, an acute spondylolysis without slippage will be observed. However, as the involved disc undergoes degeneration secondary to increased shear forces, a low-grade slip will develop (Figure 6). This is termed a spondylolytic spondylolisthesis, reflecting the traumatic etiology of the slip.

Figure 5
Figure 5:
A and B, radiographs of a patient with acquired spondylolytic spondylolisthesis. The morphology of the lumbosacral junction is normal with the exception of the bilateral stress fractures of the L5 pars interarticularis.
Figure 6
Figure 6:
A and B, lateral radiographs of a patient with a low dysplastic slip demonstrate progression due to degeneration of the intervertebral disc.

A number of radiographic parameters have been used to describe the anatomic spatial relationship between L5 and the sacrum.48 The Meyerding classification divides a slip into four grades (I, II, III, IV) depending on the severity of translation. This is a simple method, easily understood, and the most widely used. A combination of the Marchetti-Bartolozzi classification system with an anatomic descriptor, such as the Meyerding classification, can convey an accurate image of the spondylolisthesis.

The postsurgical, pathologic, and degenerative types of spondylolisthesis are similar to those in Newman’s classification.49 Postsurgical spondylolisthesis is divided into direct and indirect. A direct postsurgical spondylolisthesis may result from posterior decompression or disc surgery at the level of subsequent slippage. An indirect slippage may occur at a level superior to previous surgery such as a short lumbosacral fusion; or distal to a long thoracolumbar fusion for scoliosis. Indirect postsurgical spondylolisthesis is observed as part of the so-called transition syndrome.

Pathologic spondylolisthesis is subdivided into local and systemic processes. Local pathologic spondylolisthesis is secondary to a focal process at the involved level. Systemic pathologic spondylolisthesis is the result of a generalized bone or connective tissue disorder such as osteogenesis imperfecta, Ehler-Danlos disease, or Marfan’s syndrome.

Degenerative spondylolisthesis is categorized as primary or secondary. The prototype for primary degenerative spondylolisthesis is the typical degenerative spondylolisthesis observed in a middle-aged woman. Secondary degenerative spondylolisthesis is found in patients with a predisposing factor for degenerative changes such as at the level above a congenital fusion.

Conclusion

The acute traumatic, postsurgical, pathologic, and degenerative types of spondylolisthesis are usually recognized as inherently different and treated accordingly. Unfortunately, developmental and spondylolytic, or “isthmic,” spondylolisthesis in adolescents and young adults have been grouped and discussed together. As a consequence, the natural histories of these processes have been obscured, resulting in confusion over the appropriate treatments. The two pathologies share a similar initial radiographic deformity, but the etiologies and natural histories are clearly different, necessitating different clinical expectations and treatments.

The natural history of high dysplastic developmental spondylolisthesis is much more progressive than the spondylolytic form. The Marchetti and Bartolozzi classification system makes the distinction between the two types, permitting early recognition and treatment.40 Certainly, all would agree that the surgical treatment of a low grade slip is preferable to any operative procedure for a spondyloptosis.

Key Points

  • The posterior elements play a key role in resisting the high shear forces at the lumbosacral junction. The loss of posterior restraint can result in spondylolisthesis.
  • The spinopelvic relationships also have role in the development and progression of spondylolisthesis, although the exact nature is not yet clearly defined.
  • The Marchetti-Bartolozzi classification system differentiates between developmental and acquired forms of spondylolisthesis. The system recognizes that, although both dysplastic slips and acquired pars stress fractures may demonstrate isthmic defects, the former are more disposed to severe progression.
  • A growth deficiency of the anterosuperior sacrum may be an important factor in the progression of dysplastic spondylolisthesis.

References

1.Dandy DJ, Shannon MJ. Lumbo-sacral subluxation (Group I spondylolisthesis). J Bone Joint Surg Br 1971;53:578–95.
2.Schwab FJ, Farcy JPC, Roye DP Jr. The sagittal pelvic tilt index as a criterion in the evaluation of spondylolisthesis. Spine 1997;22:1661–7.
3.Bernhardt M, Bridwell KH. Segmental analysis of the sagittal plane alignment of the normal thoracic and lumbar spines and the thoracolumbar junction. Spine 1989;14:717–21.
4.Jackson RP, McManus AC. Radiographic analysis of sagittal plane alignment and balance in standing volunteers and patients with low back pain matched for age, sex, and size. Spine 1994;19:1611–8.
5.Stagnara P, DeMauroy JC, Dram G, et al. Reciprocal angulation of vertebral bodies in a sagittal plane: approach to references for the evaluation of the kyphosis and lordosis. Spine 1982;7:335–42.
6.Louis R. Surgery of the Spine: Surgical Anatomy and Operative Approaches. New York: Springer Verlag, 1983.
7.Antonaides SB, Hammerberg KW, DeWald RL. Sagittal plane configuration of the sacrum in spondylolisthesis. Spine 2000;25:1085–91.
8.Duval-Beaupere G, Boisaubert B, Hecquet J, et al. Sagittal profile of normal spine changes in spondylolisthesis. In: Harms J, Sturz H, eds. Severe Spondylolisthesis. Darmstadt, Germany: Steinkopff Verlag, 2000:21–32.
9.Curylo LJ, Edwards C, DeWald RL. Radiographic markers in spondyloptosis: implications for spondylolisthesis progression. Spine 2002;27:2021–5.
10.Hanson DS, Bridwell KH, Rhee JM, et al. Correlation of pelvic incidence with low- and high-grade isthmic spondylolisthesis. Spine 2002;27:2026–9.
11.Jackson RP, Phipps T, Hales C, et al. Pelvic lordosis and alignment in spondylolisthesis. Spine 2003;28:151–60.
12.Pearcy MJ, Tibrewal SB. Axial rotation and lateral bending in the normal lumbar spine measured by three-dimensional radiography. Spine 1984;9:582–7.
13.Pearcy M, Roftek I, Shepherd J. Three-dimensional analysis of normal movement in the lumbar spine. Spine 1984;9:294–7.
14.White AA, Panjabi MM. The basic kinematics of the human spine: a review of past and current knowledge. Spine 1978;3:12–20.
15.Yamamoto I, Panjabi MM, Crisco JJ, et al. Three-dimensional movements of the whole lumbar spine and lumbosacral joint. Spine 1989;14:1256–60.
16.Nachemson A. The load on lumbar disks in different positions of the body. Clin Orthop 1966;45:107–22.
17.Nachemson AL, Schultz AB, Berkson MH. Mechanical properties of human lumbar spine motion segments. Spine 1979;4:1–8.
18.Bell GH, Dunbar O, Beck JS, et al. Variation in strength of lumbar vertebrae with age and their relationship to osteoporosis. Calcif Tissue Res 1967;1:75.
19.Brown T, Hansen RJ, Yowa A. Some mechanical tests lumbosacral spine with particular references to the intervertebral discs. J Bone Joint Surg Am 1957;39:1135–64.
20.Perry O. Resistance and compression of the lumbar vertebrae. In: Encyclopedia of Medical Radiology. New York: Springer Verlag, 1974.
21.Andersson GBJ. The biomechanics of the posterior elements of the lumbar spine. Spine 1983;8:326.
22.Cyron BM, Hutton WC, Troup JDG. Spondylolytic fractures. J Bone Joint Surg Br 1976;58:462–6.
23.Troup JDG. Mechanical factors in spondylolisthesis and spondylolysis. Clin Orthop 1976;117:59–67.
24.Farfan HF, Osteria V, Lamy C. The mechanical etiology of spondylolysis and spondylolisthesis. Clin Orthop 1976;117:40–58.
25.Troup JDG. The etiology of spondylolysis. Orthop Clin North Am 1977;8:57–63.
26.Adams MA, Hutton WC. The effect of posture on the role of the apophyseal joints in resisting intervertebral compressive forces. J Bone Joint Surg Br 1980;62:358–62.
27.Fiorini GY, McCammond D. Forces of the lumbovertebral facets. Ann Biomed Eng 1976;4:354–63.
28.Hakin NS, King AI. Static and dynamic articular facet loads. Proceedings of the Twentieth Staff Conference (Dearborn mid October), 1976:609–39.
29.Yang KH, King AI. Mechanism of facet load transmission as a hypothesis for low back pain. Spine 1984;9:557–65.
30.Miller JAA, Hadenspeck KA, Schultz AB. Posterior element loads in lumbar motion segments. Spine 1983;8:331–7.
31.Adams MA, Hutton WC. The mechanical function of the lumbar apophyseal joints. Spine 1983;8:327–30.
32.Haher TR, O’Brien M, Dryer JW, et al. The role of the lumbar facet joint in spinal stability: identification of alternative paths of loading. Spine 1994;19:2667–71.
33.Oxland TR, Crisco JJ, Panjabi MM. The effect of injury on rotational coupling at the lumbosacral joint: a biomechanical investigation. Spine 1992;17:74–9.
34.Cyron BM, Hutton WC. The fatigue strength of the lumbar neural arch in spondylolysis. J Bone Joint Surg Br 1978;60:234–8.
35.Lamy C, Bazerqui A, Kraus H, et al. The strength of the neural arch and the etiology of spondylolysis. Orthop Clin North Am 1975;6:215–31.
36.Stewart TD. The age incidence of neural arch defects in Alaskan natives considered from the viewpoint of etiology. J Bone Joint Surg Am 1966;46:498–502.
37.Jayson MIV. Compression stresses in the posterior elements and pathologic consequences. Spine 1983;8:338–9.
38.Shah JS, Hampson WGJ, Jayson MIV. The distribution of surface strain in the cadaveric lumbar spine. J Bone Joint Surg Br 1978;60:246–51.
39.Green TP, Allvery JC, Adams MA. Spondylolysis: bending of the inferior articular process of lumbar vertebrae during simulated spinal movements. Spine 1994;19:2683–91.
40.Marchetti PG, Bartolozzi P. Spondylolisthesis: classification of spondylolisthesis as a guideline for treatment. In: The Textbook of Spinal Surgery, 2nd ed. Philadelphia: Lippincott-Raven, 1997:1211–54.
41.Bradford DS, Kahmann RD, Erikson D, et al. Lumbosacral kyphosis, tethered cord, and diplomyelia: a newly described neuro-ectodermal triad. Presented at the Scoliosis Research Society 23rd Annual Meeting, Baltimore, 1988:97.
42.Lindholm TS, Ragui P, Ylikoski M, et al. Lumbar isthmic spondylolisthesis in children and adolescents: radiographic evaluation and results of operative treatment. Spine 1990;16:1350–5.
43.Ikata T, Miyake R, Katoh S, et al. Pathogenesis of sports-related spondylolisthesis in adolescents: radiographic and magnetic imaging study. Am J Sports Med 1996;24:94–8.
44.Takahashi K, Yamagata M, Takayanagi K, et al. Changes in the sacrum in severe spondylolisthesis: a possible key pathology of the disorder. J Sci Orthop 2000;5:18–24.
45.Kajiura K, Katoh S, Sairyo K, et al. Slippage mechanism of pediatric spondylolysis: biomechanical study using immature calf spines. Spine 2001;26:2208–13.
46.Sakamaki T, Sairyo K, Katoh S, et al. The pathogenesis of slippage and deformity in the pediatric lumbar spine: a radiographic and histiologic study using a new rat in vivo model. Spine 2002;28:645–50.
47.Schoenecker PL, Cole HO, Herring JA, et al. Cauda equina syndrome following in situ arthrodesis of severe spondylolisthesis of the lumbosacral junction. J Bone Joint Surg Am 1990;72:369–77.
48.Hammerberg KW. Spondylolysis and spondylolisthesis. In: DeWald RL, ed. Spinal Deformities: The Comprehensive Text. New York: Thieme, 2003:787–800.
49.Newman PH, Stone KH. The etiology of spondylolisthesis. J Bone Joint Surg Br 1963;45:39–59.
Keywords:

high dysplastic developmental spondylolisthesis; acquired spondylitic spondylolisthesis; Marchetti-Bartolozzi classification; kyphospondylolisthesis; pelvic incidence

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