Contribution of postoperative vertebral remodeling to reversal of vertebral wedging and prevention of correction loss in patients with adolescent Scheuermann’s kyphosis

Sinian Wang MD1, Liang Xu MD1, Muyi Wang MD1, Yong Qiu MD1, Zezhang Zhu MD1, Bin Wang MD1, and Xu Sun MD1
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  • 1 Spine Surgery, Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
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OBJECTIVE

This study aimed to investigate reversal of vertebral wedging and to evaluate the contribution of vertebral remodeling to correction maintenance in patients with adolescent Scheuermann’s kyphosis (SK) after posterior-only instrumented correction.

METHODS

A retrospective cohort study of patients with SK was performed. In total, 45 SK patients aged 10–20 years at surgery were included. All patients received at least 24 months of follow-up and had Risser sign greater than grade 4 at latest follow-up. Patients with Risser grade 3 or less at surgery were assigned to the low-Risser group, whereas those with Risser grade 4 or 5 were assigned to the high-Risser group. Radiographic data and patient-reported outcomes were collected preoperatively, immediately postoperatively, and at latest follow-up and compared between the two groups.

RESULTS

Remarkable postoperative correction of global kyphosis was observed, with similar correction rates between the two groups (p = 0.380). However, correction loss was slightly but significantly less in the low-Risser group during follow-up (p < 0.001). The ratio between anterior vertebral body height (AVBH) and posterior vertebral body height (PVBH) of deformed vertebrae notably increased in SK patients from postoperation to latest follow-up (p < 0.05). Loss of correction of global kyphosis was significantly and negatively correlated with increased AVBH/PVBH ratio. Compared with the high-Risser group, the low-Risser group had significantly greater increase in AVBH/PVBH ratio during follow-up (p < 0.05). The two groups had similar preoperative and postoperative Scoliosis Research Society–22 questionnaire scores for all domains.

CONCLUSIONS

Obvious reversal in wedge deformation of vertebrae was observed in adolescent SK patients. Patients with substantial growth potential had greater vertebral remodeling and less correction loss. Structural remodeling of vertebral bodies has a positive effect and protects against correction loss. These results could be help guide treatment decision-making.

ABBREVIATIONS

AVBH = anterior vertebral body height; DWA = disc wedging angle; GK = global kyphosis; LIV = lowermost instrumented vertebra; MDV = most deformed vertebra; PVBH = posterior vertebral body height; SK = Scheuermann’s kyphosis; SRS-22 = Scoliosis Research Society–22 questionnaire; UIV = uppermost instrumented vertebra; VWA = vertebral wedging angle.

OBJECTIVE

This study aimed to investigate reversal of vertebral wedging and to evaluate the contribution of vertebral remodeling to correction maintenance in patients with adolescent Scheuermann’s kyphosis (SK) after posterior-only instrumented correction.

METHODS

A retrospective cohort study of patients with SK was performed. In total, 45 SK patients aged 10–20 years at surgery were included. All patients received at least 24 months of follow-up and had Risser sign greater than grade 4 at latest follow-up. Patients with Risser grade 3 or less at surgery were assigned to the low-Risser group, whereas those with Risser grade 4 or 5 were assigned to the high-Risser group. Radiographic data and patient-reported outcomes were collected preoperatively, immediately postoperatively, and at latest follow-up and compared between the two groups.

RESULTS

Remarkable postoperative correction of global kyphosis was observed, with similar correction rates between the two groups (p = 0.380). However, correction loss was slightly but significantly less in the low-Risser group during follow-up (p < 0.001). The ratio between anterior vertebral body height (AVBH) and posterior vertebral body height (PVBH) of deformed vertebrae notably increased in SK patients from postoperation to latest follow-up (p < 0.05). Loss of correction of global kyphosis was significantly and negatively correlated with increased AVBH/PVBH ratio. Compared with the high-Risser group, the low-Risser group had significantly greater increase in AVBH/PVBH ratio during follow-up (p < 0.05). The two groups had similar preoperative and postoperative Scoliosis Research Society–22 questionnaire scores for all domains.

CONCLUSIONS

Obvious reversal in wedge deformation of vertebrae was observed in adolescent SK patients. Patients with substantial growth potential had greater vertebral remodeling and less correction loss. Structural remodeling of vertebral bodies has a positive effect and protects against correction loss. These results could be help guide treatment decision-making.

In Brief

Researchers aimed to evaluate the contribution of vertebral remodeling to reversal of vertebral wedging in patients with Scheuermann's kyphosis (SK) after posterior-only instrumented correction. For SK patients who underwent posterior correction, the biomechanical environment of the vertebral bodies around the most deformed vertebra improved significantly, and obvious reversal in wedge deformation of vertebrae was observed. This study provides important reference data for determination of timing of surgery for skeletally immature SK patients.

Scheuermann’s kyphosis (SK) is a form of adolescent structural hyperkyphosis of the thoracic or thoracolumbar spine,1 with a reported prevalence of 1%–8.3%.2 SK is often diagnosed in adolescent boys or girls presenting with a typical cosmetic back deformity, including at least three consecutive vertebral bodies wedged 5° or more and multilevel endplate irregularities or Schmorl nodes. Previous studies in the literature support use of bracing treatment for skeletally immature patients with mild to moderate kyphosis.3 However, surgical intervention during early life may be indicated for patients with clinical symptoms or progressive kyphosis, usually defined as thoracic kyphosis greater than 70° or thoracolumbar kyphosis greater than 50°.2,4 In recent years, posterior-only instrumentation and fusion via Ponte osteotomy has been the most common treatment of young patients with SK.5

Generally, the immature vertebral column grows according to the Hueter-Volkmann principle, regardless of treatment options such as observation, bracing, or surgical intervention. According to this principle, asymmetrical growth of the vertebral body is due to asymmetrical loading on ring apophyses, thereby modulating longitudinal growth. Increased pressure retards growth, and conversely, reduced pressure accelerates growth. A previous study on anterior vertebral tethering in patients with idiopathic scoliosis and appropriate growth potential found that the wedging shapes of vertebrae reversed themselves after surgery.6 For adolescent patients with SK, can reducing stress on the anterior column of the thoracolumbar spine modify the growth of vertebrae and reverse wedging deformation of vertebral bodies? To the best of our knowledge, no studies have addressed this question.

Therefore, we performed a retrospective study to investigate reversal of vertebral wedging in SK patients after posterior correction and fusion. The main objectives of this study were 3-fold: 1) evaluate the contribution of vertebral remodeling to reversal of vertebral wedging in SK patients after posterior-only instrumented correction; 2) compare the results of vertebral remodeling between patients with and without substantial growth potential; and 3) explore the effectiveness of vertebral remodeling on prevention of correction loss. We hypothesized that the initially wedged vertebrae would change to a close-to-normal shape with time after surgery.

Methods

Patients

After approval by our IRB, the medical records of a consecutive series of patients with SK who had undergone correction surgery between 2009 and 2017 were obtained from our database on the basis of the following criteria: 1) age between 10 and 20 years at surgery and the triradiate cartilage had closed; 2) diagnosis of SK based on radiological criteria (at least three adjacent vertebral bodies with a minimum of 5° of wedging) with additional findings (e.g., Schmorl nodes, endplate irregularities);7,8 3) thoracic kyphosis greater than 70° or thoracolumbar kyphosis greater than 50°; 4) treatment with posterior multiple-segment Ponte osteotomy and pedicle screw–based instrumentation; and 5) at least 24 months of follow-up and Risser sign greater than grade 4 at latest follow-up. Exclusion criteria included 1) any other sagittal-alignment spinal abnormality in addition to SK; 2) coronal curve exceeding 20°; 3) previous spinal trauma or posture injury; and 4) posterior procedure with pedicle subtraction osteotomy.

In this study, the Risser sign was used as an indicator of vertebral immaturity. Risser grade 4 or 5 has been found to indicate near cessation of vertebral longitudinal growth, whereas the vertebral body has remarkable growth potential in patients with Risser grade 3 or less.9–11 Therefore, the current cohort was divided into two groups on the basis of Risser sign: the low-Risser group (patients with Risser grade 3 or less) and the high-Risser group (patients with Risser grade 4 or 5). For all included patients, demographic data were obtained from medical records, and surgical data were collected from surgical reports.

Surgical Strategy

The surgical procedure for each patient treated at our center was performed by a single surgical team with monitoring of somatosensory evoked potentials and motor evoked potentials. The upper-end vertebra or the supraadjacent level was selected as the uppermost instrumented vertebra (UIV), and the sagittal stable vertebra or the first lordotic vertebra was selected as the lowermost instrumented vertebra (LIV).12–15

Multilevel Ponte osteotomy (usually 3–5 levels) was performed after complete exposure of the spine, with resection of supraspinous and interspinous ligaments, ligamentum flavum, and whole facet joints. Next, pedicle screws were inserted at the expected fusion levels. With respect to instrumentation, a standard two-rod construct was used before January 2012; thereafter, satellite rods were routinely added to long rods and implanted with duet screws.13 Precontoured rods were placed into these screws in the distal-to-proximal direction to cantilever the spine out of kyphosis. Then, multiple rounds of compression were performed in the area with Ponte osteotomy to strengthen the correction of kyphosis. Final tightening was performed, and posterior fusion with local and allogeneic bone was completed.

Radiographic Measurements

Measurements were performed on long-cassette, full-length, lateral standard radiographs of the entire spine before surgery, after surgery, and at latest follow-up. All parameters were measured twice by an independent observer, and the mean values were used in the analysis. Partially deformed vertebrae within the instrumentation compression level, including the most deformed vertebra (MDV), second vertebra above MDV (MDV-2), first vertebra above MDV (MDV-1), first vertebra below MDV (MDV+1), and second vertebra below MDV (MDV+2), were selected for measurement in all patients. For comparison, we also measured the vertebrae nearest to but outside instrumentation. However, detection of the nearest vertebra above UIV (UIV-1) was obstructed by the arm and soft tissue and could not be observed clearly in some patients. Thus, the nearest vertebra below LIV (LIV+1) was selected for measurement. Anterior vertebral body height (AVBH) and posterior vertebral body height (PVBH) were measured on sagittal radiographs using Surgimap version 2.1.2 (Nemaris, Inc.). AVBH was defined as the distance between the most anterior points on the superior and inferior endplates of the vertebral body, and PVBH was defined as the distance between the most posterior points on the superior and inferior endplates (Fig. 1). Afterward, the AVBH/PVBH ratio was calculated.16–18 Global kyphosis (GK) was measured as the angle between the upper- and lower-most tilted end vertebrae, and correction rate was defined as ([preoperative GK − postoperative GK]/preoperative GK × 100%).19 By marking the vertebral endplate on lateral radiographs, we measured the disc wedging angle (DWA) and vertebral wedging angle (VWA) at each segment from MDV-2 to MDV+2 (Fig. 1). By convention, lordosis was expressed as a negative value.20

FIG. 1.
FIG. 1.

Radiographs obtained immediately after surgery (A) and at latest follow-up (B) of patients with SK who underwent posterior-only multilevel Ponte osteotomy and pedicle screw instrumentation and fusion. The most wedged vertebral body was selected as the MDV. The MDV, supraadjacent and inferoadjacent segments, and LIV+1 were selected for measurement. The double-headed arrows represent AVBH and PVBH. The angles formed by the dotted lines represent periapical DWA and VWA.

Patient-Reported Outcomes

Patient-reported outcomes were assessed using the Scoliosis Research Society–22 questionnaire (SRS-22). Each patient independently completed SRS-22 preoperatively, postoperatively, and at latest follow-up.

Statistical Analysis

All analyses were performed using SPSS version 24.0 (IBM Corp.). Statistics data were expressed as mean ± SD. All data had a normal distribution according to the test of normality. The paired t-test was performed for intragroup comparisons between immediately postoperative and latest follow-up data. The Student t-test was used to evaluate parameters between groups. The chi-square test or Fisher exact test was used for analysis of categorical data. Pearson correlation analysis was used to evaluate correlations between normally distributed parameters. In this study, p values < 0.05 were considered statistically significant.

Results

Patient Characteristics

A total of 45 SK patients were included in this study, with 26 patients in the low-Risser group and 19 patients in the high-Risser group. The mean ± SD (range) age at surgery was 14.5 ± 1.4 (13–16) years in the low-Risser group and 18.2 ± 1.9 (16–20) years in the high-Risser group. The mean Risser grades in these groups were 2.3 ± 0.7 and 4.6 ± 0.5, respectively. As shown in Table 1, both groups had similar numbers of fusion levels (11.4 ± 1.9 vs 11.7 ± 2.1, p = 0.452) and similar follow-up durations (3.0 ± 1.1 years vs 2.6 ± 0.8 years, p = 0.182). There were no significant differences in location of UIV (p = 0.706) and LIV (p = 0.973) between the low-Risser and high-Risser groups. The MDV locations in the low-Risser group were T8 in 2 patients, T9 in 3, T10 in 7, T11 in 10, and T12 in 4; in the high-Risser group, these locations were T8 in 1 patient, T9 in 3, T10 in 6, T11 in 7, and T12 in 2.

TABLE 1.

Demographic data and radiographic features of the included patients

CharacteristicLow-Risser Group (n = 26)High-Risser Group (n = 19)p Value
Age at surgery, yrs14.5 ± 1.4 (13–16)18.2 ± 1.9 (16–20)<0.001
Risser grade2.3 ± 0.7 (1–3)4.6 ± 0.5 (4–5)<0.001
Sex
 Male21160.766
 Female53
FU, yrs3.0 ± 1.1 (2–5)2.6 ± 0.8 (2–4)0.182
Fusion levels11.4 ± 1.9 (10–13)11.7 ± 2.1 (10–13)0.452
MDV location
 T8210.970
 T933
 T1076
 T11107
 T1242
UIV location
 T2530.706
 T3128
 T434
 T532
 T612
 T720
LIV location
 L1220.973
 L297
 L3139
 L421
GK, °
 Preop71.1 ± 13.170.1 ± 14.60.571
 Postop36.8 ± 7.737.5 ± 7.40.882
 Latest FU37.8 ± 8.540.2 ± 8.20.126
Correction rate, %
 Postop48.2 ± 7.246.9 ± 6.90.380
 Latest FU46.8 ± 6.442.7 ± 6.10.047
Correction loss at final FU, °0.9 ± 0.72.6 ± 1.4<0.001

FU = follow-up.

Values are shown as mean ± SD (range) or number unless indicated otherwise.

Correction Results

Both groups experienced significant correction after surgery. The average postoperative GK was 36.8° ± 7.7° in the low-Risser group and 37.5° ± 7.4° in the high-Risser group. There was no significant difference between the two groups in terms of the mean correction rates (48.2% ± 7.2% vs 46.9% ± 6.9%, respectively; p = 0.380). However, correction loss was slightly but significantly lower in the low-Risser group than the high Risser-group during follow-up (0.9° ± 0.7° vs 2.6° ± 1.4°, p < 0.001), and the mean final correction rate was slightly but significantly higher in the low-Risser group (46.8% ± 6.4% vs 42.7% ± 6.1%, p = 0.047; Table 1).

Vertebral Body Remodeling

As shown in Table 2, the mean AVBH of MDV was 18.23 mm after surgery and increased to 22.50 mm at latest follow-up (p < 0.001); the average increase in AVBH was 24%. In contrast, the average increase in PVBH was 3% (from 29.62 mm after surgery to 30.32 mm at latest follow-up). The average postoperative AVBH/PVBH ratio of MDV was 0.62. At latest follow-up, this ratio increased to 0.74. Such a significant change in the AVBH/PVBH ratio indicated remarkable remodeling in wedge deformation of MDV.

TABLE 2.

Comparisons of radiographic features between postoperation and latest follow-up in SK patients (n = 45)

FeaturePostopLatest FUp Value
MDV-2
 AVBH, mm21.06 ± 3.2623.67 ± 3.11<0.001
 PVBH, mm26.30 ± 3.0127.50 ± 2.820.012
 AVBH/PVBH ratio0.80 ± 0.060.84 ± 0.06<0.001
MDV-1
 AVBH, mm20.11 ± 3.6223.04 ± 2.93<0.001
 PVBH, mm27.90 ± 3.7929.03 ± 3.180.067
 AVBH/PVBH ratio0.73 ± 0.060.79 ± 0.05<0.001
MDV
 AVBH, mm18.23 ± 3.2822.50 ± 4.36<0.001
 PVBH, mm29.62 ± 4.4830.32 ± 4.710.130
 AVBH/PVBH ratio0.62 ± 0.060.74 ± 0.06<0.001
MDV+1
 AVBH, mm21.41 ± 3.0725.26 ± 3.82<0.001
 PVBH, mm30.58 ± 4.2131.74 ± 4.750.071
 AVBH/PVBH ratio0.70 ± 0.050.79 ± 0.06<0.001
MDV+2
 AVBH, mm24.75 ± 3.2127.54 ± 3.50<0.001
 PVBH, mm32.03 ± 4.5533.36 ± 4.360.011
 AVBH/PVBH ratio0.77 ± 0.060.82 ± 0.04<0.001
LIV+1
 AVBH, mm31.44 ± 3.8232.83 ± 3.760.026
 PVBH, mm32.07 ± 4.1333.00 ± 4.540.043
 AVBH/PVBH ratio0.98 ± 0.050.99 ± 0.040.117
VWA
 MDV-2, °6.5 ± 2.34.1 ± 2.10.062
 MDV-1, °10.7 ± 3.37.6 ± 2.80.003
 MDV, °17.1 ± 2.79.3 ± 2.2<0.001
 MDV+1, °14.7 ± 2.58.8 ± 1.80.001
 MDV+2, °11.5 ± 2.06.9 ± 1.30.002
DWA
 3rd disc above MDV, °−3.5 ± 1.5−2.3 ± 1.20.044
 2nd disc above MDV, °−5.8 ± 2.1−4.0 ± 1.80.016
 1st disc above MDV, °−8.9 ± 1.4−3.5 ± 1.60.001
 1st disc below MDV, °−12.4 ± 2.5−5.4 ± 2.3<0.001
 2nd disc below MDV, °−16.1 ± 2.5−11.1 ± 2.60.003
 3rd disc below MDV, °−14.7 ± 3.5−10.7 ± 2.70.008

Values are shown as mean ± SD unless indicated otherwise.

From postoperation to latest follow-up, remodeling changes were also observed at the supraadjacent and inferoadjacent segments (p < 0.05). However, the AVBH/PVBH ratio remained steady at LIV+1 during follow-up (from 0.98 to 0.99, p = 0.117; Table 2).

Regarding angular measurements, MDV showed significant changes in shape during follow-up, with VWA decreasing from 17.1° ± 2.7° to 9.3° ± 2.2°. VWA decreased with a similar trend at the supraadjacent and inferoadjacent segments. At the same time, DWA increased significantly at the discs around MDV (Table 2).

As demonstrated by correlation analysis, less correction loss was observed as reversal of vertebral wedging increased (r = −0.570, p = 0.012). Specifically, correction loss was significantly and negatively correlated with increase in AVBH/PVBH ratio at MDV-1 (r = −0.498, p = 0.036), MDV (r = −0.742, p = 0.005), and MDV+1 (r = −0.483, p = 0.041; Table 3).

TABLE 3.

Correlation between rate of increase in AVBH/PVBH ratio and correction loss at evaluated vertebrae

Vertebrar Valuep Value
MDV-2−0.1170.526
MDV-1−0.4980.036
MDV−0.7420.005
MDV+1−0.4830.041
MDV+2−0.2400.179
Total change−0.5700.012

Comparisons of Remodeling Between Groups

Changes in the AVBH/PVBH ratios of the low- and high-Risser groups are summarized in Table 4. Similar AVBH/PVBH ratios were observed immediately after surgery between the two groups, but at latest follow-up, the low-Risser group had a significantly higher AVBH/PVBH ratio at all segments than the high-Risser group (p < 0.05). Of note, between-group differences in AVBH/PVBH ratio at LIV+1 were not significant from postoperation to latest follow-up.

TABLE 4.

Comparison of radiographic features between the low-Risser and high-Risser groups

FeatureLow-Risser GroupHigh-Risser Groupp Value
AVBH/PVBH ratio
 MDV-2
  Postop0.79 ± 0.050.78 ± 0.070.417
  Latest FU0.85 ± 0.050.82 ± 0.050.043
  Rate, %7.9 ± 3.74.9 ± 2.40.024
 MDV-1
  Postop0.72 ± 0.070.73 ± 0.050.206
  Latest FU0.80 ± 0.040.77 ± 0.040.024
  Rate, %14.6 ± 5.75.7 ± 2.20.007
 MDV
  Postop0.60 ± 0.060.63 ± 0.050.069
  Latest FU0.77 ± 0.040.70 ± 0.060.002
  Rate, %28.3 ± 9.111.5 ± 3.2<0.001
 MDV+1
  Postop0.68 ± 0.070.71 ± 0.040.137
  Latest FU0.81 ± 0.040.77 ± 0.040.025
  Rate, %18.4 ± 5.98.0 ± 3.40.002
 MDV+2
  Postop0.76 ± 0.050.77 ± 0.030.323
  Latest FU0.84 ± 0.050.80 ± 0.030.010
  Rate, %10.6 ± 4.93.1 ± 0.80.005
 LIV+1
  Postop0.97 ± 0.050.99 ± 0.050.163
  Latest FU0.98 ± 0.030.99 ± 0.040.283
  Rate, %1.1 ± 0.10.4 ± 0.10.105
Change in VWA
 MDV-2, °−2.3 ± 0.7−1.7 ± 0.60.431
 MDV-1, °−3.6 ± 1.2−2.3 ± 0.70.035
 MDV, °−9.2 ± 3.7−5.1 ± 1.90.007
 MDV+1, °−7.1 ± 3.3−4.3 ± 1.60.012
 MDV+2, °−5.2 ± 2.4−2.9 ± 0.90.047
 Total change, °−27.8 ± 6.2−15.9 ± 4.4<0.001
Change in DWA
 3rd disc above MDV, °1.2 ± 0.71.0 ± 0.30.663
 2nd disc above MDV, °2.4 ± 1.21.1 ± 0.80.129
 1st disc above MDV, °6.1 ± 1.84.3 ± 1.70.024
 1st disc below MDV, °8.1 ± 2.95.6 ± 3.80.015
 2nd disc below MDV, °6.0 ± 3.43.7 ± 2.00.021
 3rd disc below MDV, °5.0 ± 2.42.7 ± 1.70.043
 Total change, °28.6 ± 5.218.4 ± 6.2<0.001

Values are show as mean ± SD unless indicated otherwise.

Both groups showed similar increases in AVBH/PVBH ratio, which mainly occurred in the MDV segment and gradually decreased toward the cephalad or caudal ends. From immediately postoperation to latest follow-up, the average increase in AVBH/PVBH ratio at MDV was only 11.5% ± 3.2% in the high-Risser group, compared with 28.3% ± 9.1% in the low-Risser group. Increases in AVBH/PVBH ratio at MDV and the supraadjacent and inferoadjacent segments were significantly different between groups (p < 0.05).

The changes in VWA and DWA of both groups between postoperation and latest follow-up are summarized in Table 4, indicating that the absolute VWA and DWA values of the low-Risser group decreased by significantly more than those of the high-Risser group (p < 0.001; Figs. 2 and 3).

FIG. 2.
FIG. 2.

Radiographs of a 14-year-old boy with SK. A and B: The Risser sign was grade 2, and the MDV was located at T11. Before surgery, the patient had severe thoracolumbar kyphosis (75.3°). C and D: Radiographs show posterior-only multilevel Ponte osteotomies from T9 to L1 and pedicle screw instrumentation and fusion from T5 to L3. E and F: Follow-up radiographs obtained at 4 years show correction of GK to 33.3° and maintenance of correction in both coronal and sagittal planes. The AVBH/PVBH ratio of the MDV increased remarkably from 0.59 (D) to 0.78 (F).

FIG. 3.
FIG. 3.

Radiographs of an 18-year-old patient with SK. A and B: Radiographs show Risser sign grade 5 and the MDV located at T11. Before surgery, the patient had severe thoracolumbar kyphosis (73.4°). C and D: Radiographs show posterior-only multilevel Ponte osteotomies from T9 to L1 and pedicle screw instrumentation and fusion from T5 to L3. E and F: Follow-up radiographs obtained at 4 years show correction of GK to 41.9° and maintenance of correction in both coronal and sagittal planes. The AVBH/PVBH ratio of the MDV increased only from 0.59 (D) to 0.66 (F).

Patient-Reported Outcomes

The distribution of SRS-22 scores is summarized in Table 5. There were no significant differences in any preoperative, postoperative, and follow-up SRS-22 assessments between the low-Risser and high-Risser groups (p > 0.05).

TABLE 5.

Comparison of patient-reported outcomes and complications between the low-Risser and high-Risser groups

CharacteristicLow-Risser GroupHigh-Risser Groupp Value
SRS-22 score
 Pain
  Preop2.3 ± 0.42.4 ± 0.30.865
  Postop4.4 ± 0.54.5 ± 0.70.546
  Latest FU4.2 ± 0.44.3 ± 0.50.877
 Self-image
  Preop1.9 ± 0.61.8 ± 0.70.612
  Postop4.5 ± 0.34.5 ± 0.50.583
  Latest FU4.6 ± 0.54.7 ± 0.40.205
 Function/activity
  Preop3.8 ± 0.73.7 ± 0.90.563
  Postop4.0 ± 0.43.9 ± 0.50.670
  Latest FU4.2 ± 0.44.1 ± 0.50.156
 Mental health
  Preop3.5 ± 0.63.3 ± 0.50.141
  Postop4.3 ± 0.44.3 ± 0.60.954
  Latest FU4.3 ± 0.54.2 ± 0.60.526
 Satisfaction
  Preop
  Postop4.4 ± 0.54.2 ± 0.50.134
  Latest FU4.4 ± 0.54.3 ± 0.40.344
Complications
 Fat liquefaction & delayed wound healing1 (3.8)1 (5.3)0.820
 Nut loosening1 (15.4)00.387
 PJK4 (15.4)6 (31.6)0.197
 DJK2 (7.7)2 (10.5)0.741

DJK = distal junctional kyphosis; PJK = proximal junctional kyphosis. Values are shown as mean ± SD or number (percent) unless indicated otherwise.

Complications

At latest follow-up, 8 patients in the low-Risser group and 9 patients in the high-Risser group had experienced surgery-related complications. One patient in the low-Risser group and 1 patient in the high-Risser group experienced fat liquefaction and delayed wound healing. Both patients were successfully treated with dressing change. One patient in the low-Risser group had nut loosening. Proximal junctional kyphosis was identified in 4 patients in the low-Risser group and 6 in the high-Risser group (p = 0.197). Two patients in the low-Risser group had distal junctional kyphosis, whereas 2 patients in the high-Risser group had this pathology (p = 0.741). Neurological complications and pseudarthrosis were not observed in any patients (Table 5).

Discussion

This study retrospectively reviewed 45 SK patients who underwent posterior-only correction and fusion via Ponte osteotomy. Our results indicated that wedging of deformed vertebrae was significantly reversed during postoperative follow-up in SK patients. Patients in the low-Risser group, as compared with those in the high-Risser group, experienced greater vertebral remodeling and less correction loss during minimum 2-year follow-up. In addition, vertebral remodeling had a positive effect on reducing correction loss.

The data in our study show that the anterior column of deformed vertebrae can grow significantly and surpass the posterior column after posterior-only correction via multilevel Ponte osteotomy in patients with SK. Because the correction maneuver anteriorly opens intervertebral discs, asymmetrical growth may be due to decreased stress on the anterior segment of the deformed vertebrae, as evidenced by the biomechanical effect of the Hueter-Volkmann principle on vertebral remodeling.

Spinal remodeling via modification of mechanical forces according to the Hueter-Volkmann principle has been investigated with several animal models.21–24 Braun et al.23 reported on a variety of scoliosis implant strategies tested in the rat tail model. Their results demonstrated that dynamic loading of vertebrae provided the greatest potential for growth regulation. Meanwhile, preservation of the growth potential of the vertebrae is an attractive option for the treatment of spinal deformity.25,26 Olgun et al.27 studied growth stimulation for individual vertebrae in scoliosis patients who underwent treatment with growing rod. They found that the vertebrae in the instrumented segment grew faster than the corresponding lower lumbar vertebrae lying outside the instrumented segment. Ahmad et al.28 also demonstrated that posterior tethering in skeletally immature patients decreased pressure on highly stressed parts, with the potential to promote vertebral remodeling while correcting scoliosis. These findings corroborated the application of the Hueter-Volkmann principle for the treatment of scoliosis.

In our study, utilization of the posterior instrumented correction technique helped to decrease pressure on the highly stressed parts of the growing vertebrae. After surgery, periapical DWA increased, which decreased the huge pressure that was initially concentrated on the anterior parts of vertebral bodies and provided them with ample space for growth. Consequently, we found significant remodeling of vertebral wedging that was in line with the Hueter-Volkmann principle. In kyphosis curves, reduced compression on the anterior side of the curve modulated vertebral growth, whereas growth on the posterior side was inhibited owing to increased compression.29 Interestingly, we observed little vertebral remodeling in the high-Risser group. A previous study also demonstrated that some patients with Risser sign grade 4 had growth activity in vertebral growth plates.30 Therefore, in our study, the AVBH/PVBH ratio of the deformed vertebrae within the instrumented compression level in SK patients was close to or exceeded the normal ratio at latest follow-up, which had been reported as between 0.83 and 0.85 for lower thoracic vertebrae.31 As a result, the wedging shapes of the deformed vertebrae were dramatically reversed.

Significant correlations were also found between increased AVBH/PVBH ratio and correction loss at the latest follow-up. During Ponte osteotomy, the posterior element is closed and the anterior element is opened through the intervertebral disc space to achieve correction.32 Correction loss during follow-up could be mainly due to the inability to provide the support needed to maintain correction, which results from anterior opening and deformation of the disc spaces. Vertebral remodeling resulting from the biomechanical effects of the Hueter-Volkmann principle helps to reduce DWA and to stabilize the anterior segment of the spine. The correlation between rate of increase in AVBH/PVBH ratio and correction loss means that vertebral remodeling according to the Hueter-Volkmann principle played an important role in prevention of correction loss.

In our study, we observed similar kyphosis correction rates immediately after surgery regardless of skeletal maturity. However, our results showed that the SK patients in the low-Risser group, as compared with those in the high-Risser group, had greater vertebral remodeling and less correction loss over a follow-up period of at least 2 years; this difference may be related to differences in vertebral body remodeling and may further increase with time. As a result, greater changes in DWA from postoperation to latest follow-up were observed in the low-Risser group than the high-Risser group. Therefore, remarkable vertebral remodeling was significantly correlated with reduced correction loss. Yet, a previous study observed unacceptable correction loss and implant breakage due to anterior opening of intervertebral discs in kyphosis patients treated with posterior-only correction; thus, additional anterior fusion was suggested as necessary to achieve correction and solid fusion.33 Nevertheless, our study found that vertebral remodeling significantly decreased postoperative anterior opening of discs in the low-Risser group, as compared with that in the high-Risser group. Our findings imply that correction stability can always be ensured with vertebral remodeling after instrumented posterior fusion in skeletally immature patients with kyphosis, and these patients do not usually need additional anterior surgery, even if there is significant opening of the intervertebral discs. Previously, some authors advocated bracing treatment for skeletally immature patients, in order to wait until after the skeleton has matured to perform subsequent surgical interventions.34,35 However, our study indicates that posterior fusion surgery should be performed when indicated and there is no need to wait until skeletal maturity, because better vertebral remodeling and less correction loss can be obtained in patients with low Risser grade.

On the basis of our results, it is reasonable to believe that vertebral remodeling in SK patients is consistent with the Hueter-Volkmann principle. By comparing the patients in the high-Risser group with those in the low-Risser group, our study highlighted that vertebral maturity may be an important factor in predicting prognosis of SK correction. Postoperative vertebral remodeling in skeletally immature patients with SK contributes to stabilization of the anterior part of the curve, thereby diminishing correction loss due to anterior opening of the intervertebral space after surgery. To some extent, SK patients with substantial growth potential may be good candidates for posterior correction and fusion.

This study has several limitations. First, this study was a relatively small case series. Second, Risser grade is not considered a highly precise predictor of vertebral growth, but it is still a reliable indicator for predicting residual growth potential of the spine.36 Third, this was a short-term study. However, all SK patients had Risser sign grade 4 or 5 at latest follow-up. Thus, a long-term study needs to be conducted to observe the impact of vertebral remodeling on clinical outcomes and postoperative complications. Last, only radiography was used as a radiographic assessment tool, which may be inferior to CT in terms of imaging quality, but this protocol minimized radiation exposure and financial burden on patients.

Conclusions

The biomechanical environment of the vertebral bodies around MDV improved significantly in SK patients who underwent posterior correction via Ponte osteotomy, and obvious reversal in wedge deformation of the vertebrae was also observed. Compared with the patients in the high-Risser group, the patients in the low-Risser group had greater vertebral remodeling and less correction loss. Structural remodeling of vertebral bodies has a positive effect and protects against correction loss. This study provides important reference data for determination of timing of surgery and surgical approach for skeletally immature patients with SK.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant no. 81772422) and the Natural Science Foundation of Jiangsu Province (BE2017606).

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Sun, S Wang, Qiu. Acquisition of data: S Wang, Xu, M Wang. Analysis and interpretation of data: Sun, S Wang, Xu, M Wang. Drafting the article: S Wang. Critically revising the article: Sun. Reviewed submitted version of manuscript: Sun. Statistical analysis: S Wang. Administrative/technical/material support: Qiu, Zhu, B Wang. Study supervision: Qiu, Zhu, B Wang.

References

  • 1

    Scheuermann HW. The classic: kyphosis dorsalis juvenilis.Clin Orthop Relat Res. 1977;(128):57.

  • 2

    Lowe TG, Line BG. Evidence based medicine: analysis of Scheuermann kyphosis. Spine (Phila Pa 1976).2007;32(19)(suppl):S115S119.

  • 3

    Palazzo C, Sailhan F, Revel M. Scheuermann’s disease: an update. Joint Bone Spine. 2014;81(3):209214.

  • 4

    Lowe TG. Scheuermann’s kyphosis. Neurosurg Clin N Am. 2007;18(2):305315.

  • 5

    Lee SS, Lenke LG, Kuklo TR, et al. Comparison of Scheuermann kyphosis correction by posterior-only thoracic pedicle screw fixation versus combined anterior/posterior fusion. Spine (Phila Pa 1976).2006;31(20):23162321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Newton PO, Kluck DG, Saito W, et al. Anterior spinal growth tethering for skeletally immature patients with scoliosis: a retrospective look two to four years postoperatively. J Bone Joint Surg Am. 2018;100(19):16911697.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Faldini C, Traina F, Perna F, et al. Does surgery for Scheuermann kyphosis influence sagittal spinopelvic parameters?. Eur Spine J. 2015;24(suppl 7):893897.

  • 8

    Jiang L, Qiu Y, Xu L, et al. Sagittal spinopelvic alignment in adolescents associated with Scheuermann’s kyphosis: a comparison with normal population. Eur Spine J. 2014;23(7):14201426.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Noordeen MH, Haddad FS, Edgar MA, Pringle J. Spinal growth and a histologic evaluation of the Risser grade in idiopathic scoliosis. Spine (Phila Pa 1976).1999;24(6):535538.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Wang WW, Xia CW, Zhu F, et al. Correlation of Risser sign, radiographs of hand and wrist with the histological grade of iliac crest apophysis in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976).2009;34(17):18491854.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Zhu Z, Tang NL, Xu L, et al. Genome-wide association study identifies new susceptibility loci for adolescent idiopathic scoliosis in Chinese girls. Nat Commun. 2015;6:8355.

  • 12

    Geck MJ, Macagno A, Ponte A, Shufflebarger HL. The Ponte procedure: posterior only treatment of Scheuermann’s kyphosis using segmental posterior shortening and pedicle screw instrumentation. J Spinal Disord Tech. 2007;20(8):586593.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zhu ZZ, Chen X, Qiu Y, et al. Adding satellite rods to standard two-rod construct with the use of duet screws: an effective technique to improve surgical outcomes and preventing proximal junctional kyphosis in posterior-only correction of Scheuermann kyphosis. Spine (Phila Pa 1976).2018;43(13):E758E765.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Xu L, Shi B, Qiu Y, et al. How does the cervical spine respond to hyperkyphosis correction in Scheuermann’s disease?. J Neurosurg Spine. 2019;31(4):493500.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Zhu W, Sun X, Pan W, et al. Curve patterns deserve attention when determining the optimal distal fusion level in correction surgery for Scheuermann kyphosis. Spine J. 2019;19(9):15291539.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Goh S, Price RI, Leedman PJ, Singer KP. A comparison of three methods for measuring thoracic kyphosis: implications for clinical studies. Rheumatology (Oxford). 2000;39(3):310315.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Manns RA, Haddaway MJ, McCall IW, et al. The relative contribution of disc and vertebral morphometry to the angle of kyphosis in asymptomatic subjects. Clin Radiol. 1996;51(4):258262.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Goh S, Price RI, Leedman PJ, Singer KP. The relative influence of vertebral body and intervertebral disc shape on thoracic kyphosis. Clin Biomech (Bristol, Avon). 1999;14(7):439448.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Koller H, Juliane Z, Umstaetter M, et al. Surgical treatment of Scheuermann’s kyphosis using a combined antero-posterior strategy and pedicle screw constructs: efficacy, radiographic and clinical outcomes in 111 cases. Eur Spine J. 2014;23(1):180191.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Tsutsui S, Pawelek JB, Bastrom TP, et al. Do discs “open” anteriorly with posterior-only correction of Scheuermann’s kyphosis?. Spine (Phila Pa 1976).2011;36(16):E1086E1092.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Akyuz E, Braun JT, Brown NA, Bachus KN. Static versus dynamic loading in the mechanical modulation of vertebral growth. Spine (Phila Pa 1976).2006;31(25):E952E958.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Braun JT, Hoffman M, Akyuz E, et al. Mechanical modulation of vertebral growth in the fusionless treatment of progressive scoliosis in an experimental model. Spine (Phila Pa 1976).2006;31(12):13141320.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Braun JT, Hines JL, Akyuz E, et al. Relative versus absolute modulation of growth in the fusionless treatment of experimental scoliosis. Spine (Phila Pa 1976).2006;31(16):17761782.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Mente PL, Aronsson DD, Stokes IA, Iatridis JC. Mechanical modulation of growth for the correction of vertebral wedge deformities. J Orthop Res. 1999;17(4):518524.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Harrington PR. Treatment of scoliosis. Correction and internal fixation by spine instrumentation. J Bone Joint Surg Am. 1962;44-A:591610.

  • 26

    Moe JH. Modern concepts of treatment of spinal deformities in children and adults. Clin Orthop Relat Res. 1980;(150):137153.

  • 27

    Olgun ZD, Ahmadiadli H, Alanay A, Yazici M. Vertebral body growth during growing rod instrumentation: growth preservation or stimulation?. J Pediatr Orthop. 2012;32(2):184189.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Ahmad AA, Aker L, Hanbali Y, et al. Growth modulation and remodeling by means of posterior tethering technique for correction of early-onset scoliosis with thoracolumbar kyphosis. Eur Spine J. 2017;26(6):17481755.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Mehlman CT, Araghi A, Roy DR. Hyphenated history: the Hueter-Volkmann law. Am J Orthop. 1997;26(11):798800.

  • 30

    Wang S, Qiu Y, Ma Z, et al. Histologic, Risser sign, and digital skeletal age evaluation for residual spine growth potential in Chinese female idiopathic scoliosis. Spine (Phila Pa 1976).2007;32(15):16481654.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Scoles PV, Latimer BM, DiGiovanni BF, et al. Vertebral alterations in Scheuermann’s kyphosis. Spine (Phila Pa 1976).1991;16(5):509515.

  • 32

    Ponte A, Orlando G, Siccardi GL. The true Ponte osteotomy: by the one who developed it. Spine Deform. 2018;6(1):211.

  • 33

    Böhm H, Harms J, Donk R, Zielke K. Correction and stabilization of angular kyphosis. Clin Orthop Relat Res. 1990;(258):5661.

  • 34

    Tribus CB. Scheuermann’s kyphosis in adolescents and adults: diagnosis and management. J Am Acad Orthop Surg. 1998;6(1):3643.

  • 35

    Marty C, Boisaubert B, Descamps H, et al. The sagittal anatomy of the sacrum among young adults, infants, and spondylolisthesis patients. Eur Spine J. 2002;11(2):119125.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Wang SF, Qiu Y, Zhu ZZ, et al. Assessment of the residual spine growth potential in idiopathic scoliosis by Risser sign and histological grading. Article in Chinese. Zhonghua Yi Xue Za Zhi. 2008;88(7):461464.

    • PubMed
    • Search Google Scholar
    • Export Citation

Illustration from Rothrock et al. (pp 535–545). Copyright Roberto Suazo. Published with permission.

  • View in gallery

    Radiographs obtained immediately after surgery (A) and at latest follow-up (B) of patients with SK who underwent posterior-only multilevel Ponte osteotomy and pedicle screw instrumentation and fusion. The most wedged vertebral body was selected as the MDV. The MDV, supraadjacent and inferoadjacent segments, and LIV+1 were selected for measurement. The double-headed arrows represent AVBH and PVBH. The angles formed by the dotted lines represent periapical DWA and VWA.

  • View in gallery

    Radiographs of a 14-year-old boy with SK. A and B: The Risser sign was grade 2, and the MDV was located at T11. Before surgery, the patient had severe thoracolumbar kyphosis (75.3°). C and D: Radiographs show posterior-only multilevel Ponte osteotomies from T9 to L1 and pedicle screw instrumentation and fusion from T5 to L3. E and F: Follow-up radiographs obtained at 4 years show correction of GK to 33.3° and maintenance of correction in both coronal and sagittal planes. The AVBH/PVBH ratio of the MDV increased remarkably from 0.59 (D) to 0.78 (F).

  • View in gallery

    Radiographs of an 18-year-old patient with SK. A and B: Radiographs show Risser sign grade 5 and the MDV located at T11. Before surgery, the patient had severe thoracolumbar kyphosis (73.4°). C and D: Radiographs show posterior-only multilevel Ponte osteotomies from T9 to L1 and pedicle screw instrumentation and fusion from T5 to L3. E and F: Follow-up radiographs obtained at 4 years show correction of GK to 41.9° and maintenance of correction in both coronal and sagittal planes. The AVBH/PVBH ratio of the MDV increased only from 0.59 (D) to 0.66 (F).

  • 1

    Scheuermann HW. The classic: kyphosis dorsalis juvenilis.Clin Orthop Relat Res. 1977;(128):57.

  • 2

    Lowe TG, Line BG. Evidence based medicine: analysis of Scheuermann kyphosis. Spine (Phila Pa 1976).2007;32(19)(suppl):S115S119.

  • 3

    Palazzo C, Sailhan F, Revel M. Scheuermann’s disease: an update. Joint Bone Spine. 2014;81(3):209214.

  • 4

    Lowe TG. Scheuermann’s kyphosis. Neurosurg Clin N Am. 2007;18(2):305315.

  • 5

    Lee SS, Lenke LG, Kuklo TR, et al. Comparison of Scheuermann kyphosis correction by posterior-only thoracic pedicle screw fixation versus combined anterior/posterior fusion. Spine (Phila Pa 1976).2006;31(20):23162321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Newton PO, Kluck DG, Saito W, et al. Anterior spinal growth tethering for skeletally immature patients with scoliosis: a retrospective look two to four years postoperatively. J Bone Joint Surg Am. 2018;100(19):16911697.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Faldini C, Traina F, Perna F, et al. Does surgery for Scheuermann kyphosis influence sagittal spinopelvic parameters?. Eur Spine J. 2015;24(suppl 7):893897.

  • 8

    Jiang L, Qiu Y, Xu L, et al. Sagittal spinopelvic alignment in adolescents associated with Scheuermann’s kyphosis: a comparison with normal population. Eur Spine J. 2014;23(7):14201426.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Noordeen MH, Haddad FS, Edgar MA, Pringle J. Spinal growth and a histologic evaluation of the Risser grade in idiopathic scoliosis. Spine (Phila Pa 1976).1999;24(6):535538.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Wang WW, Xia CW, Zhu F, et al. Correlation of Risser sign, radiographs of hand and wrist with the histological grade of iliac crest apophysis in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976).2009;34(17):18491854.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Zhu Z, Tang NL, Xu L, et al. Genome-wide association study identifies new susceptibility loci for adolescent idiopathic scoliosis in Chinese girls. Nat Commun. 2015;6:8355.

  • 12

    Geck MJ, Macagno A, Ponte A, Shufflebarger HL. The Ponte procedure: posterior only treatment of Scheuermann’s kyphosis using segmental posterior shortening and pedicle screw instrumentation. J Spinal Disord Tech. 2007;20(8):586593.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zhu ZZ, Chen X, Qiu Y, et al. Adding satellite rods to standard two-rod construct with the use of duet screws: an effective technique to improve surgical outcomes and preventing proximal junctional kyphosis in posterior-only correction of Scheuermann kyphosis. Spine (Phila Pa 1976).2018;43(13):E758E765.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Xu L, Shi B, Qiu Y, et al. How does the cervical spine respond to hyperkyphosis correction in Scheuermann’s disease?. J Neurosurg Spine. 2019;31(4):493500.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Zhu W, Sun X, Pan W, et al. Curve patterns deserve attention when determining the optimal distal fusion level in correction surgery for Scheuermann kyphosis. Spine J. 2019;19(9):15291539.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Goh S, Price RI, Leedman PJ, Singer KP. A comparison of three methods for measuring thoracic kyphosis: implications for clinical studies. Rheumatology (Oxford). 2000;39(3):310315.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Manns RA, Haddaway MJ, McCall IW, et al. The relative contribution of disc and vertebral morphometry to the angle of kyphosis in asymptomatic subjects. Clin Radiol. 1996;51(4):258262.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Goh S, Price RI, Leedman PJ, Singer KP. The relative influence of vertebral body and intervertebral disc shape on thoracic kyphosis. Clin Biomech (Bristol, Avon). 1999;14(7):439448.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Koller H, Juliane Z, Umstaetter M, et al. Surgical treatment of Scheuermann’s kyphosis using a combined antero-posterior strategy and pedicle screw constructs: efficacy, radiographic and clinical outcomes in 111 cases. Eur Spine J. 2014;23(1):180191.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Tsutsui S, Pawelek JB, Bastrom TP, et al. Do discs “open” anteriorly with posterior-only correction of Scheuermann’s kyphosis?. Spine (Phila Pa 1976).2011;36(16):E1086E1092.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Akyuz E, Braun JT, Brown NA, Bachus KN. Static versus dynamic loading in the mechanical modulation of vertebral growth. Spine (Phila Pa 1976).2006;31(25):E952E958.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Braun JT, Hoffman M, Akyuz E, et al. Mechanical modulation of vertebral growth in the fusionless treatment of progressive scoliosis in an experimental model. Spine (Phila Pa 1976).2006;31(12):13141320.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Braun JT, Hines JL, Akyuz E, et al. Relative versus absolute modulation of growth in the fusionless treatment of experimental scoliosis. Spine (Phila Pa 1976).2006;31(16):17761782.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Mente PL, Aronsson DD, Stokes IA, Iatridis JC. Mechanical modulation of growth for the correction of vertebral wedge deformities. J Orthop Res. 1999;17(4):518524.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Harrington PR. Treatment of scoliosis. Correction and internal fixation by spine instrumentation. J Bone Joint Surg Am. 1962;44-A:591610.

  • 26

    Moe JH. Modern concepts of treatment of spinal deformities in children and adults. Clin Orthop Relat Res. 1980;(150):137153.

  • 27

    Olgun ZD, Ahmadiadli H, Alanay A, Yazici M. Vertebral body growth during growing rod instrumentation: growth preservation or stimulation?. J Pediatr Orthop. 2012;32(2):184189.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Ahmad AA, Aker L, Hanbali Y, et al. Growth modulation and remodeling by means of posterior tethering technique for correction of early-onset scoliosis with thoracolumbar kyphosis. Eur Spine J. 2017;26(6):17481755.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Mehlman CT, Araghi A, Roy DR. Hyphenated history: the Hueter-Volkmann law. Am J Orthop. 1997;26(11):798800.

  • 30

    Wang S, Qiu Y, Ma Z, et al. Histologic, Risser sign, and digital skeletal age evaluation for residual spine growth potential in Chinese female idiopathic scoliosis. Spine (Phila Pa 1976).2007;32(15):16481654.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Scoles PV, Latimer BM, DiGiovanni BF, et al. Vertebral alterations in Scheuermann’s kyphosis. Spine (Phila Pa 1976).1991;16(5):509515.

  • 32

    Ponte A, Orlando G, Siccardi GL. The true Ponte osteotomy: by the one who developed it. Spine Deform. 2018;6(1):211.

  • 33

    Böhm H, Harms J, Donk R, Zielke K. Correction and stabilization of angular kyphosis. Clin Orthop Relat Res. 1990;(258):5661.

  • 34

    Tribus CB. Scheuermann’s kyphosis in adolescents and adults: diagnosis and management. J Am Acad Orthop Surg. 1998;6(1):3643.

  • 35

    Marty C, Boisaubert B, Descamps H, et al. The sagittal anatomy of the sacrum among young adults, infants, and spondylolisthesis patients. Eur Spine J. 2002;11(2):119125.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Wang SF, Qiu Y, Zhu ZZ, et al. Assessment of the residual spine growth potential in idiopathic scoliosis by Risser sign and histological grading. Article in Chinese. Zhonghua Yi Xue Za Zhi. 2008;88(7):461464.

    • PubMed
    • Search Google Scholar
    • Export Citation

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