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SPINE Volume 34, Number 25, pp 2782–2786
                                                                                                        ©2009, Lippincott Williams & Wilkins


         Cobb Angle Progression in Adolescent Scoliosis Begins
         at the Intervertebral Disc

         Ryan E. Will, MD,* Ian A. Stokes, PhD,† Xing Qiu, PhD,‡ Matthew R. Walker, MSc,*
         and James O. Sanders, MD‡


                                                                           Scoliosis progression during the adolescent growth spurt
       Study Design. Longitudinal radiographic study of pa-                is poorly understood. Various investigators have at-
   tients with progressive idiopathic scoliosis.                           tempted to identify the specific etiology of curve progres-
       Objective. To determine the relative contributions of
                                                                           sion, but the results have been inconclusive. Part of this is
   vertebral and disc wedging to the increase in Cobb
   angle during 3 phases of adolescent skeletal growth                     because reliable comparison of patients at the same stage
   and maturation.                                                         of curve progression has been impossible. The high cor-
       Summary of Background Data. Both disc wedging                       relation of the digital skeletal age (DSA) with the curve
   and vertebral body wedging are found in progressive                     acceleration phase (CAP) in adolescent idiopathic scoli-
   scoliosis, but their relative contribution to curve pro-
                                                                           osis provides an opportunity to make appropriate com-
   gression over time is unknown. Which occurs first is
   important for understanding how scoliosis progresses                    parisons between patients.1 Although both discs and ver-
   and for developing methods to halt progression. Previ-                  tebrae deform in progressive scoliosis, the relative
   ous studies have not properly identified maturity, and                   contribution of each to Cobb angle progression has not
   provide conflicting results.                                             been demonstrated. It is thought that both the discs and
       Methods. Eighteen girls were followed through their
                                                                           vertebrae become increasingly wedged as a result of
   adolescent growth spurt with serial spine and hand skel-
   etal age radiographs. Each Cobb angle was divided into                  asymmetrical loading and asymmetrical growth.2,3
   disc wedge angles and vertebral wedge angles. The cor-                     In this study, patients with adolescent idiopathic sco-
   responding hand radiographs provided a measure of ma-                   liosis (AIS) at a similar maturity level were compared
   turity level, the Digital Skeletal Age (DSA). The disc versus           during their adolescent growth spurt to identify whether
   bone contributions to the Cobb angle were then com-
   pared during 3 growth phases: before the growth spurt,
                                                                           the Cobb angle progresses through the vertebra or
   during the growth spurt and after the growth spurt. Sig-                through the intervertebral disc. Changes primarily in the
   nificance of relative changes was assessed with the Wil-                 vertebra, measured as vertebral wedging, imply that
   coxon 2-sided mean rank test.                                           growth inhibition on the concavity of the curve is the
       Results. Before the growth spurt, there was no dif-                 primary cause for scoliosis progression. Changes primar-
   ference in relative contributions of the disc and the
   bone (3° vs. 0°, P      0.38) to curve progression. During
                                                                           ily in the disc, measured as disc wedging, imply that an
   the growth spurt, the mean disc component progressed                    unknown process in the soft tissue is the principal cause
   significantly more than that of the vertebrae (15° vs. 0°,               for scoliosis progression. The aim of this study was to
   P     0.0002). This reversed following the growth spurt                 determine whether the contributions of disc and verte-
   with the vertebral component progressing more than                      bral wedging to the progression of scoliosis differed be-
   the disc (10° vs. 0°, P      0.01).
                                                                           fore, during and after the growth spurt.
       Conclusion. Adolescent idiopathic scoliosis initially in-
   creases through disc wedging during the rapid growth                       Materials and Methods
   spurt with progressive vertebral wedging occurring later.
       Key words: adolescent idiopathic scoliosis, progres-                This study population was the same as that in the study of
   sion, skeletal maturity, vertebral wedging, intervertebral              Sanders et all in which a cohort of 22 girls with AIS was fol-
   disc wedging. Spine 2009;34:2782–2786                                   lowed through their growth spurt with serial PA spine radio-
                                                                           graphs, serial skeletal age radiographs, and a number of clinical
                                                                           and biochemical markers of maturation obtained every 6
                                                                           months. Patients were braced according to accepted criteria
From the *Shriners Hospitals for Children, Erie PA; †Department of
Orthopaedics, University of Vermont, Burlington, VT; and ‡Depart-          and instructed to wear the brace 23 hours per day. Bracing was
ment of Orthopaedics and Rehabilitation, University of Rochester,          initiated for curves with a Cobb angle of 25° or more or a Cobb
Rochester, NY.                                                             angle of 20° to 24° with documented 5° progression in patients
Acknowledgment date: June 11, 2008. Revision date: November 17,            with a Risser sign of 2 or less. The curve type for each patient
2008. Acceptance date: November 17, 2008.
                                                                           was classified according to a modified Lenke classification4
The manuscript submitted does not contain information about medical
device(s)/drug(s).                                                         (Table 1). Of the original cohort, 18 subjects had sufficient
Professional Organizational funds were received in support of this work.
No benefits in any form have been or will be received from a commercial
party related directly or indirectly to the subject of this manuscript.
Supported by NIH R01AR 053132 (to I.A.F.S.) and a grant from the           Table 1. Distribution of Type of Scoliosis Curves
Scoliosis Research Society (to J.O.S.).                                    (Lenke4 Classification)
IRB review and approval obtained.
Address for correspondence and reprint requests to James O. Sanders,                 Type 1    Type 2      Type 3    Type 4    Type 5    Type 6
MD, Department of Orthopaedics and Rehabilitation, University of
Rochester, 601 Elmwood Ave, Rochester, NY 14642; E-mail:                   Number       6        2            4         1         4         1
james_sanders@urmc.rochester.edu

2782
Cobb Angle Progression • Will et al 2783

                                                                         acceleration phase (CAP). DSA greater than 450 was consid-
                                                                         ered the postcurve acceleration phase.1 The values of disc and
                                                                         vertebral wedge angles were averaged for each maturity point
                                                                         and compared to each other.
                                                                             Statistical analysis by 2 sample, 2 sided Wilcoxon rank sum
                                                                         test was used to compare the changes on the relative amount of
                                                                         disc and vertebral wedging between each of the 4 maturity
                                                                         points. All statistical analyses were done by using the R pro-
                                                                         gramming language (R Foundation for Statistical Computing,
                                                                         Vienna, Austria).

                                                                            Results
Figure 1. Disc Cobb angle is the sum contribution of “D” and ver-
tebral Cobb angle the sum contribution of “V” to the total Cobb angle.   An average of 8.1 2.5 spine radiographs were obtained
                                                                         per patient. The average initial Cobb angle was 25.6°
progression to warrant inclusion in this current study. Only             10.7° (range: 11.6 – 46.5) and the average final Cobb angle
curves with more than 10° of progression were included.                  was 53.3° 16.1° (range: 28.4 – 82.3). The average curve
    Each spine radiograph was digitized and saved as a digital           progression was 27.7° (range: 11.1– 61.9). The initial aver-
image file. An operator used custom software5 to record the               age age was 10.8 1.4 years and the average final age was
positions of 2 points on each of the superior and inferior ver-          14.5 0.8 years. Average follow-up time was 3.7 1.3
tebral endplates of each vertebral body from T1 to L5 for each           years.
spine radiograph. The relative inclinations of lines passing                The results of disc wedging and vertebral wedging
through these points provided a measurement of the vertebral             compared to DSA for all patients are shown in Figures 2
wedge angle and disc wedge angle for each level (Figure 1). The
                                                                         and 3, respectively. For disc wedge angles, the average
reliability of the measurement technique was evaluated by ex-
                                                                         change pre-CAP (before DSA 375) was 3°. CAP average
amining data from a previous study6 of inter- and intraobserver
reliability, using the same computer-assisted radiographic mea-          change (from DSA 375 to 450) was 15°. Post-CAP (after
surement. The tilt angles of the vertebral endplates were mea-           DSA 450) average change was 0°. For the vertebral
sure with a mean overall standard deviation of 1.6° (values              wedge angles, the average change pre-CAP was 0°. CAP
ranged from 1.45° to 1.9° for 4 observers). The interobserver            average change was 0°. Post-CAP average change was
variability of the Cobb angles (angle between maximally tilted           10°. The difference in disc and vertebral wedging contri-
endplates) was 1.6°. The total Cobb angle for a major curve              butions to curve progression were significant during CAP
was the sum of the disc wedge angles and vertebral wedge                 (P     0.0002) and after CAP (P         0.01). P-values in
angles for the levels of that curve. For each patient, the total         parentheses were obtained from Wilcoxon rank sum test
Cobb angle, total disc wedge angle, and total vertebral wedge            comparing the 2 subgroups.
angle were graphed against the digital skeletal age (DSA).1 The
                                                                            Disc wedge angle increases were greatest during the
time axis of these graphs was divided into 3 phases correspond-
                                                                         rapid curve progression in the CAP, while vertebral
ing to the 3 main stages of growth: precurve acceleration phase,
curve acceleration phase (CAP), and postcurve acceleration               wedge angle increased primarily after the CAP. This pat-
phase. Four DSA measurements were selected to define the 3                tern of early curve progression through the disc, and later
phases of growth: less than 375, 375, 450, and greater than              curve progression occurring in the vertebra is evident in
450. DSA less than 375 was considered the precurve accelera-             the percent of Cobb angle values for the cohort of pa-
tion phase. DSA from 375 to 450 was considered the curve                 tients, as shown in Table 2. Figure 4 is the graphical




Figure 2. Disc contribution to
the Cobb angle longitudinally
compared to skeletal maturity.
2784 Spine • Volume 34 • Number 25 • 2009




Figure 3. Vertebral body contri-
bution to the Cobb angle longitudi-
nally compared to skeletal maturity.


representation of the significant differences between disc                     discs and vertebrae were unchanged. However, in that
and vertebral wedging, during the 3 maturity phases.                          study, maturity markers were not used to identify when
                                                                              or if the subject was in the rapid growth phase that usu-
   Discussion
                                                                              ally accompanies curve progression. Grivas et al9 mea-
In this population of patients with progressive AIS, it was                   sured radiographs of 70 patients with scoliosis in a cross-
found that spinal deformity begins with changes in the                        sectional study. Similar to our findings, vertebral
intervertebral discs, during the most rapid phase of                          wedging was found to increase after the Cobb angle in-
growth. Vertebral changes occurred after the discs have                       creased. Importantly, the disc wedge angle was the ra-
deformed, and growth decreases. Thus, the anatomic lo-                        diographic parameter most closely associated with curve
cation where Cobb angle progression occurred, differed                        progression, again consistent with our findings. How-
by maturity level. It changed from a process occurring                        ever, only the apex and the levels immediately above and
primarily located at the intervertebral disc before and                       below the apex were measured, and maturity markers
during the growth spurt to a process occurring primarily                      were not used. In MRI studies, increasing scoliosis has
at the vertebral bodies after the growth spurt.                               been associated with displacement of the nucleus pulpo-
   This study focused on the development of wedging                           sus towards the convex side.10,11
deformity by means of a longitudinal study design with a                          It has been suggested that the while idiopathic scolio-
cohort of patients with progressive scoliosis. Most prior                     sis is probably initiated by unknown extraspinal fac-
studies of vertebral and disc wedging have been cross                         tors,12 the progression of the deformity, once it reaches a
sectional and have not been able to stratify by maturity                      certain magnitude, occurs primarily through the action
appropriately. In prior radiographic studies, Perdriolle3                     of asymmetrical forces on growing bone and soft issue.2
reported that there was a greater proportion of disc                          If this is true, then the mechanism by which curve pro-
wedging in smaller curves than in larger curves, and                          gression occurs in the vertebrae and discs appears to be
Xiong et al7 reported that both structures were wedged                        substantially different. This is consistent with the differ-
in curves less than 30°. Repeated radiographic measure-                       ent mechanisms of growth and remodeling that occur in
ments patients with progressive scoliosis by Stokes and                       bone and soft tissue. Most successful nonhuman models
Aronsson8 indicated that the relative contributions of the                    of scoliosis progression have created a tether, which
                                                                              spontaneously produces the disc changes. These studies
Table 2. Average Disc Wedge Angle and Vertebral                               have then concentrated on the bone deformity, empha-
Wedge Angle as a Percent of Cobb Angle at 4 Points                            sizing the Heuter-Volkman effect. In the present study,
of Digital Skeletal Age                                                       the Cobb angle for the major curve was divided into its
                                                                              vertebral and disc components with results implying that
                               Disc Wedge Angle Vertebra Wedge Angle          the bony changes are secondary and that initial progres-
Digital Skeletal Cobb Angle     (Percent of Cobb  (Percent of Cobb
Age              Percentage          Angle)             Angle)                sion occurs through the soft tissues as reflected by early
                                                                              changes in disc wedging.
Pre 375              100               51.9                  48.1                 A separate model of scoliosis progression is based on
375                  100               54.1                  45.9
450                  100               71.2                  28.8             anterior bone overgrowth compared to the posterior col-
Post 450             100               57.6                  42.4             umn as proposed by Roaf13 and Somerville.14 In a study
Note the large change in the disc wedge angle contribution from DSA 375 to    supporting this mechanism, Guo et al15 found the ante-
450, which is also the CAP. Significant vertebral changes occur after DSA of   rior column substantially longer than the posterior column
450 only.
                                                                              on a cross-sectional study compared to nonscoliotic con-
Cobb Angle Progression • Will et al 2785




Figure 4. The average Cobb an-
gle and the contribution from
both the discs and vertebral bod-
ies relative to skeletal maturity.



trols. They proposed that the primary mechanism of scoli-       lescent idiopathic scoliosis. After the growth spurt, the
osis progression is an uncoupling of the anterior endochon-     vertebral body is the primary anatomic site of Cobb an-
dral ossification from the posterior element growth.             gle progression in patients with adolescent idiopathic
However, their study did not control for maturity, and a        scoliosis. This implies that treatments designed to correct
posterior lateral tether could create the same bony finding      vertebral deformity, such as staples or tethers, may not
by later growth inhibition on the posterior concavity.          be acting in the appropriate phase of growth for maxi-
    The strengths of this present study include its longitu-    mum effectiveness.
dinal design, measurement of vertebral and disc wedge
angles for the entire major curve and measuring progres-
sion of Cobb angles in scoliosis as it relates to maturity.           Key Points
Its limitations include the relatively small sample size and      ● Progression of scoliosis as measured by the Cobb
analysis limited to the 2 dimensions of the coronal defor-          angle does not distinguish between the contribu-
mity, using plain radiographs. Because the patients were            tions of disc and vertebral wedging.
treated with braces during curve progression, the finding of       ● Using digital skeletal age as a measure of skeletal
this study may not accurately reflect the natural history of         maturity, the wedging of intervertebral discs
untreated scoliosis. However, it does reflect brace treatment        made the largest contribution to the scoliosis
criteria commonly used at the time of this study.                   progression in the interval just before and during
    The findings of the present study may help to explain            the curve acceleration phase, while vertebral
the mechanism of scoliosis progression during skeletal              wedging was the predominant source of curve
growth. The longitudinal growth in the vertebrae occurs             progression thereafter.
almost exclusively from the vertebral endplates.16 Soft           ● This study implies that the source of early rapid
tissue grows in apposition, probably in response to ten-            scoliosis progression is the surrounding soft tis-
sion but there is very little increase in height of interver-       sues rather than concave vertebral endplate
tebral discs during adolescent growth.17 The finding of              growth inhibition.
intervertebral disc deformation occurring first, followed
later by asymmetrical vertebral growth, suggests that the
disc tissue on the convex side may be placed under rela-        References
tive tension, thus stimulating its growth or remodeling,        1. Sanders JO, Browne RH, McConnell SJ, et al. Maturity assessment and curve
especially in the early stages of curve progression. Soft          progression in girls with idiopathic scoliosis. J Bone Joint Surg Am 2007;89:
                                                                   64 –73.
tissues on the convexity then grow at a relatively more         2. Roaf R. Vertebral growth and its mechanical control. J Bone Joint Surg Br
rapid rate than the concavity crating a functional con-            1960;42:40 –59.
cave tether. Because these soft tissues in the thoracic         3. Perdriolle R. La Scoliose: Son etude Tridimensionnelle. Paris, France: Mal-
                                                                                                   ´
                                                                   oine SA; 1979.
spine are primarily posterior, this accounts for the typi-      4. Lenke LG, Betz RR, Harms J, et al. Adolescent idiopathic scoliosis: a new
cal thoracic lordoscoliosis.                                       classification to determine extent of spinal arthrodesis. J Bone Joint Surg Am
    Our study demonstrates that the intervertebral disc is         2001;83-A:1169 – 81.
                                                                5. Stokes IA, Aronsson DD. Identifying sources of variability in scoliosis clas-
the primary anatomic site of rapid Cobb angle progres-             sification using a rule-based automated algorithm. Spine 2002;27:2801–5.
sion during the early growth spurt in patients with ado-        6. Stokes IA, Aronsson DD. Computer-assisted algorithms improve reliability
2786 Spine • Volume 34 • Number 25 • 2009

      of King classification and Cobb angle measurement of scoliosis. Spine 2006;            distribution within scoliotic vertebrae. Magn Reson Imaging 2003;21:
      31:665–70.                                                                            949 –53.
 7.   Xiong B, Sevastik JA, Hedlund R, et al. Radiographic changes at the coronal     12.   Enneking WF, Harrington PR. Pathological changes in scoliosis. J Bone Joint
      plane in early scoliosis. Spine 1994;19:159 – 64.                                     Surg Am 1969;51-A:165–75.
 8.   Stokes IA, Aronsson DD. Disc and vertebral wedging in patients with pro-        13.   Roaf R. The basic anatomy of scoliosis. J Bone Joint Surg Br 1966;48B:786 –92.
      gressive scoliosis. J Spinal Disord 2001;14:317–22.                             14.   Somerville EW. Rotational lordosis: the development of the single curve.
 9.   Grivas TB, Vasiliadis E, Malakasis M, et al. Intervertebral disc biomechanics         J Bone Joint Surg Br 1952;34B:421–7.
      in the pathogenesis of idiopathic scoliosis. Stud Health Technol Inform         15.   Guo X, Chau WW, Chan YL, et al. Relative anterior spinal overgrowth in
      2006;123:80 –3.                                                                       adolescent idiopathic scoliosis: results of disproportionate enchondral mem-
10.   Toyama Y. An experimental study on the pathology and role of interverte-              branous bone growth. J Bone Joint Surg Br 2003;85B:1026 –31.
      bral discs in the progression and correction of scoliotic deformity. Nippon     16.   Dickson RA, Deacon P. Spinal growth. J Bone Joint Surg Br 1987;69:
      Seikeigeka Gakkai Zasshi 1988;62:777– 89.                                             690 –2.
11.   Perie D, Curnier D, de Gauzy JS. Correlation between nucleus zone mi-           17.   Stokes IA, Windisch L. Vertebral height growth predominates over interver-
      gration within scoliotic intervertebral discs and mechanical properties               tebral disc height growth in the adolescent spine. Spine 2006;31:1600 – 4.

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Cobb Angle Progression in Adolescent Scoliosis Begins at the Intervertebral Disc

  • 1. SPINE Volume 34, Number 25, pp 2782–2786 ©2009, Lippincott Williams & Wilkins Cobb Angle Progression in Adolescent Scoliosis Begins at the Intervertebral Disc Ryan E. Will, MD,* Ian A. Stokes, PhD,† Xing Qiu, PhD,‡ Matthew R. Walker, MSc,* and James O. Sanders, MD‡ Scoliosis progression during the adolescent growth spurt Study Design. Longitudinal radiographic study of pa- is poorly understood. Various investigators have at- tients with progressive idiopathic scoliosis. tempted to identify the specific etiology of curve progres- Objective. To determine the relative contributions of sion, but the results have been inconclusive. Part of this is vertebral and disc wedging to the increase in Cobb angle during 3 phases of adolescent skeletal growth because reliable comparison of patients at the same stage and maturation. of curve progression has been impossible. The high cor- Summary of Background Data. Both disc wedging relation of the digital skeletal age (DSA) with the curve and vertebral body wedging are found in progressive acceleration phase (CAP) in adolescent idiopathic scoli- scoliosis, but their relative contribution to curve pro- osis provides an opportunity to make appropriate com- gression over time is unknown. Which occurs first is important for understanding how scoliosis progresses parisons between patients.1 Although both discs and ver- and for developing methods to halt progression. Previ- tebrae deform in progressive scoliosis, the relative ous studies have not properly identified maturity, and contribution of each to Cobb angle progression has not provide conflicting results. been demonstrated. It is thought that both the discs and Methods. Eighteen girls were followed through their vertebrae become increasingly wedged as a result of adolescent growth spurt with serial spine and hand skel- etal age radiographs. Each Cobb angle was divided into asymmetrical loading and asymmetrical growth.2,3 disc wedge angles and vertebral wedge angles. The cor- In this study, patients with adolescent idiopathic sco- responding hand radiographs provided a measure of ma- liosis (AIS) at a similar maturity level were compared turity level, the Digital Skeletal Age (DSA). The disc versus during their adolescent growth spurt to identify whether bone contributions to the Cobb angle were then com- pared during 3 growth phases: before the growth spurt, the Cobb angle progresses through the vertebra or during the growth spurt and after the growth spurt. Sig- through the intervertebral disc. Changes primarily in the nificance of relative changes was assessed with the Wil- vertebra, measured as vertebral wedging, imply that coxon 2-sided mean rank test. growth inhibition on the concavity of the curve is the Results. Before the growth spurt, there was no dif- primary cause for scoliosis progression. Changes primar- ference in relative contributions of the disc and the bone (3° vs. 0°, P 0.38) to curve progression. During ily in the disc, measured as disc wedging, imply that an the growth spurt, the mean disc component progressed unknown process in the soft tissue is the principal cause significantly more than that of the vertebrae (15° vs. 0°, for scoliosis progression. The aim of this study was to P 0.0002). This reversed following the growth spurt determine whether the contributions of disc and verte- with the vertebral component progressing more than bral wedging to the progression of scoliosis differed be- the disc (10° vs. 0°, P 0.01). fore, during and after the growth spurt. Conclusion. Adolescent idiopathic scoliosis initially in- creases through disc wedging during the rapid growth Materials and Methods spurt with progressive vertebral wedging occurring later. Key words: adolescent idiopathic scoliosis, progres- This study population was the same as that in the study of sion, skeletal maturity, vertebral wedging, intervertebral Sanders et all in which a cohort of 22 girls with AIS was fol- disc wedging. Spine 2009;34:2782–2786 lowed through their growth spurt with serial PA spine radio- graphs, serial skeletal age radiographs, and a number of clinical and biochemical markers of maturation obtained every 6 months. Patients were braced according to accepted criteria From the *Shriners Hospitals for Children, Erie PA; †Department of Orthopaedics, University of Vermont, Burlington, VT; and ‡Depart- and instructed to wear the brace 23 hours per day. Bracing was ment of Orthopaedics and Rehabilitation, University of Rochester, initiated for curves with a Cobb angle of 25° or more or a Cobb Rochester, NY. angle of 20° to 24° with documented 5° progression in patients Acknowledgment date: June 11, 2008. Revision date: November 17, with a Risser sign of 2 or less. The curve type for each patient 2008. Acceptance date: November 17, 2008. was classified according to a modified Lenke classification4 The manuscript submitted does not contain information about medical device(s)/drug(s). (Table 1). Of the original cohort, 18 subjects had sufficient Professional Organizational funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Supported by NIH R01AR 053132 (to I.A.F.S.) and a grant from the Table 1. Distribution of Type of Scoliosis Curves Scoliosis Research Society (to J.O.S.). (Lenke4 Classification) IRB review and approval obtained. Address for correspondence and reprint requests to James O. Sanders, Type 1 Type 2 Type 3 Type 4 Type 5 Type 6 MD, Department of Orthopaedics and Rehabilitation, University of Rochester, 601 Elmwood Ave, Rochester, NY 14642; E-mail: Number 6 2 4 1 4 1 james_sanders@urmc.rochester.edu 2782
  • 2. Cobb Angle Progression • Will et al 2783 acceleration phase (CAP). DSA greater than 450 was consid- ered the postcurve acceleration phase.1 The values of disc and vertebral wedge angles were averaged for each maturity point and compared to each other. Statistical analysis by 2 sample, 2 sided Wilcoxon rank sum test was used to compare the changes on the relative amount of disc and vertebral wedging between each of the 4 maturity points. All statistical analyses were done by using the R pro- gramming language (R Foundation for Statistical Computing, Vienna, Austria). Results Figure 1. Disc Cobb angle is the sum contribution of “D” and ver- tebral Cobb angle the sum contribution of “V” to the total Cobb angle. An average of 8.1 2.5 spine radiographs were obtained per patient. The average initial Cobb angle was 25.6° progression to warrant inclusion in this current study. Only 10.7° (range: 11.6 – 46.5) and the average final Cobb angle curves with more than 10° of progression were included. was 53.3° 16.1° (range: 28.4 – 82.3). The average curve Each spine radiograph was digitized and saved as a digital progression was 27.7° (range: 11.1– 61.9). The initial aver- image file. An operator used custom software5 to record the age age was 10.8 1.4 years and the average final age was positions of 2 points on each of the superior and inferior ver- 14.5 0.8 years. Average follow-up time was 3.7 1.3 tebral endplates of each vertebral body from T1 to L5 for each years. spine radiograph. The relative inclinations of lines passing The results of disc wedging and vertebral wedging through these points provided a measurement of the vertebral compared to DSA for all patients are shown in Figures 2 wedge angle and disc wedge angle for each level (Figure 1). The and 3, respectively. For disc wedge angles, the average reliability of the measurement technique was evaluated by ex- change pre-CAP (before DSA 375) was 3°. CAP average amining data from a previous study6 of inter- and intraobserver reliability, using the same computer-assisted radiographic mea- change (from DSA 375 to 450) was 15°. Post-CAP (after surement. The tilt angles of the vertebral endplates were mea- DSA 450) average change was 0°. For the vertebral sure with a mean overall standard deviation of 1.6° (values wedge angles, the average change pre-CAP was 0°. CAP ranged from 1.45° to 1.9° for 4 observers). The interobserver average change was 0°. Post-CAP average change was variability of the Cobb angles (angle between maximally tilted 10°. The difference in disc and vertebral wedging contri- endplates) was 1.6°. The total Cobb angle for a major curve butions to curve progression were significant during CAP was the sum of the disc wedge angles and vertebral wedge (P 0.0002) and after CAP (P 0.01). P-values in angles for the levels of that curve. For each patient, the total parentheses were obtained from Wilcoxon rank sum test Cobb angle, total disc wedge angle, and total vertebral wedge comparing the 2 subgroups. angle were graphed against the digital skeletal age (DSA).1 The Disc wedge angle increases were greatest during the time axis of these graphs was divided into 3 phases correspond- rapid curve progression in the CAP, while vertebral ing to the 3 main stages of growth: precurve acceleration phase, curve acceleration phase (CAP), and postcurve acceleration wedge angle increased primarily after the CAP. This pat- phase. Four DSA measurements were selected to define the 3 tern of early curve progression through the disc, and later phases of growth: less than 375, 375, 450, and greater than curve progression occurring in the vertebra is evident in 450. DSA less than 375 was considered the precurve accelera- the percent of Cobb angle values for the cohort of pa- tion phase. DSA from 375 to 450 was considered the curve tients, as shown in Table 2. Figure 4 is the graphical Figure 2. Disc contribution to the Cobb angle longitudinally compared to skeletal maturity.
  • 3. 2784 Spine • Volume 34 • Number 25 • 2009 Figure 3. Vertebral body contri- bution to the Cobb angle longitudi- nally compared to skeletal maturity. representation of the significant differences between disc discs and vertebrae were unchanged. However, in that and vertebral wedging, during the 3 maturity phases. study, maturity markers were not used to identify when or if the subject was in the rapid growth phase that usu- Discussion ally accompanies curve progression. Grivas et al9 mea- In this population of patients with progressive AIS, it was sured radiographs of 70 patients with scoliosis in a cross- found that spinal deformity begins with changes in the sectional study. Similar to our findings, vertebral intervertebral discs, during the most rapid phase of wedging was found to increase after the Cobb angle in- growth. Vertebral changes occurred after the discs have creased. Importantly, the disc wedge angle was the ra- deformed, and growth decreases. Thus, the anatomic lo- diographic parameter most closely associated with curve cation where Cobb angle progression occurred, differed progression, again consistent with our findings. How- by maturity level. It changed from a process occurring ever, only the apex and the levels immediately above and primarily located at the intervertebral disc before and below the apex were measured, and maturity markers during the growth spurt to a process occurring primarily were not used. In MRI studies, increasing scoliosis has at the vertebral bodies after the growth spurt. been associated with displacement of the nucleus pulpo- This study focused on the development of wedging sus towards the convex side.10,11 deformity by means of a longitudinal study design with a It has been suggested that the while idiopathic scolio- cohort of patients with progressive scoliosis. Most prior sis is probably initiated by unknown extraspinal fac- studies of vertebral and disc wedging have been cross tors,12 the progression of the deformity, once it reaches a sectional and have not been able to stratify by maturity certain magnitude, occurs primarily through the action appropriately. In prior radiographic studies, Perdriolle3 of asymmetrical forces on growing bone and soft issue.2 reported that there was a greater proportion of disc If this is true, then the mechanism by which curve pro- wedging in smaller curves than in larger curves, and gression occurs in the vertebrae and discs appears to be Xiong et al7 reported that both structures were wedged substantially different. This is consistent with the differ- in curves less than 30°. Repeated radiographic measure- ent mechanisms of growth and remodeling that occur in ments patients with progressive scoliosis by Stokes and bone and soft tissue. Most successful nonhuman models Aronsson8 indicated that the relative contributions of the of scoliosis progression have created a tether, which spontaneously produces the disc changes. These studies Table 2. Average Disc Wedge Angle and Vertebral have then concentrated on the bone deformity, empha- Wedge Angle as a Percent of Cobb Angle at 4 Points sizing the Heuter-Volkman effect. In the present study, of Digital Skeletal Age the Cobb angle for the major curve was divided into its vertebral and disc components with results implying that Disc Wedge Angle Vertebra Wedge Angle the bony changes are secondary and that initial progres- Digital Skeletal Cobb Angle (Percent of Cobb (Percent of Cobb Age Percentage Angle) Angle) sion occurs through the soft tissues as reflected by early changes in disc wedging. Pre 375 100 51.9 48.1 A separate model of scoliosis progression is based on 375 100 54.1 45.9 450 100 71.2 28.8 anterior bone overgrowth compared to the posterior col- Post 450 100 57.6 42.4 umn as proposed by Roaf13 and Somerville.14 In a study Note the large change in the disc wedge angle contribution from DSA 375 to supporting this mechanism, Guo et al15 found the ante- 450, which is also the CAP. Significant vertebral changes occur after DSA of rior column substantially longer than the posterior column 450 only. on a cross-sectional study compared to nonscoliotic con-
  • 4. Cobb Angle Progression • Will et al 2785 Figure 4. The average Cobb an- gle and the contribution from both the discs and vertebral bod- ies relative to skeletal maturity. trols. They proposed that the primary mechanism of scoli- lescent idiopathic scoliosis. After the growth spurt, the osis progression is an uncoupling of the anterior endochon- vertebral body is the primary anatomic site of Cobb an- dral ossification from the posterior element growth. gle progression in patients with adolescent idiopathic However, their study did not control for maturity, and a scoliosis. This implies that treatments designed to correct posterior lateral tether could create the same bony finding vertebral deformity, such as staples or tethers, may not by later growth inhibition on the posterior concavity. be acting in the appropriate phase of growth for maxi- The strengths of this present study include its longitu- mum effectiveness. dinal design, measurement of vertebral and disc wedge angles for the entire major curve and measuring progres- sion of Cobb angles in scoliosis as it relates to maturity. Key Points Its limitations include the relatively small sample size and ● Progression of scoliosis as measured by the Cobb analysis limited to the 2 dimensions of the coronal defor- angle does not distinguish between the contribu- mity, using plain radiographs. Because the patients were tions of disc and vertebral wedging. treated with braces during curve progression, the finding of ● Using digital skeletal age as a measure of skeletal this study may not accurately reflect the natural history of maturity, the wedging of intervertebral discs untreated scoliosis. However, it does reflect brace treatment made the largest contribution to the scoliosis criteria commonly used at the time of this study. progression in the interval just before and during The findings of the present study may help to explain the curve acceleration phase, while vertebral the mechanism of scoliosis progression during skeletal wedging was the predominant source of curve growth. The longitudinal growth in the vertebrae occurs progression thereafter. almost exclusively from the vertebral endplates.16 Soft ● This study implies that the source of early rapid tissue grows in apposition, probably in response to ten- scoliosis progression is the surrounding soft tis- sion but there is very little increase in height of interver- sues rather than concave vertebral endplate tebral discs during adolescent growth.17 The finding of growth inhibition. intervertebral disc deformation occurring first, followed later by asymmetrical vertebral growth, suggests that the disc tissue on the convex side may be placed under rela- References tive tension, thus stimulating its growth or remodeling, 1. Sanders JO, Browne RH, McConnell SJ, et al. Maturity assessment and curve especially in the early stages of curve progression. Soft progression in girls with idiopathic scoliosis. J Bone Joint Surg Am 2007;89: 64 –73. tissues on the convexity then grow at a relatively more 2. Roaf R. Vertebral growth and its mechanical control. J Bone Joint Surg Br rapid rate than the concavity crating a functional con- 1960;42:40 –59. cave tether. Because these soft tissues in the thoracic 3. Perdriolle R. La Scoliose: Son etude Tridimensionnelle. Paris, France: Mal- ´ oine SA; 1979. spine are primarily posterior, this accounts for the typi- 4. Lenke LG, Betz RR, Harms J, et al. Adolescent idiopathic scoliosis: a new cal thoracic lordoscoliosis. classification to determine extent of spinal arthrodesis. J Bone Joint Surg Am Our study demonstrates that the intervertebral disc is 2001;83-A:1169 – 81. 5. Stokes IA, Aronsson DD. Identifying sources of variability in scoliosis clas- the primary anatomic site of rapid Cobb angle progres- sification using a rule-based automated algorithm. Spine 2002;27:2801–5. sion during the early growth spurt in patients with ado- 6. Stokes IA, Aronsson DD. Computer-assisted algorithms improve reliability
  • 5. 2786 Spine • Volume 34 • Number 25 • 2009 of King classification and Cobb angle measurement of scoliosis. Spine 2006; distribution within scoliotic vertebrae. Magn Reson Imaging 2003;21: 31:665–70. 949 –53. 7. Xiong B, Sevastik JA, Hedlund R, et al. Radiographic changes at the coronal 12. Enneking WF, Harrington PR. Pathological changes in scoliosis. J Bone Joint plane in early scoliosis. Spine 1994;19:159 – 64. Surg Am 1969;51-A:165–75. 8. Stokes IA, Aronsson DD. Disc and vertebral wedging in patients with pro- 13. Roaf R. The basic anatomy of scoliosis. J Bone Joint Surg Br 1966;48B:786 –92. gressive scoliosis. J Spinal Disord 2001;14:317–22. 14. Somerville EW. Rotational lordosis: the development of the single curve. 9. Grivas TB, Vasiliadis E, Malakasis M, et al. Intervertebral disc biomechanics J Bone Joint Surg Br 1952;34B:421–7. in the pathogenesis of idiopathic scoliosis. Stud Health Technol Inform 15. Guo X, Chau WW, Chan YL, et al. Relative anterior spinal overgrowth in 2006;123:80 –3. adolescent idiopathic scoliosis: results of disproportionate enchondral mem- 10. Toyama Y. An experimental study on the pathology and role of interverte- branous bone growth. J Bone Joint Surg Br 2003;85B:1026 –31. bral discs in the progression and correction of scoliotic deformity. Nippon 16. Dickson RA, Deacon P. Spinal growth. J Bone Joint Surg Br 1987;69: Seikeigeka Gakkai Zasshi 1988;62:777– 89. 690 –2. 11. Perie D, Curnier D, de Gauzy JS. Correlation between nucleus zone mi- 17. Stokes IA, Windisch L. Vertebral height growth predominates over interver- gration within scoliotic intervertebral discs and mechanical properties tebral disc height growth in the adolescent spine. Spine 2006;31:1600 – 4.