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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 2  |  Issue : 2  |  Page : 114-121

Treatment of scoliosis in osteogenesis imperfecta: Experience at a single institution


1 Department of Orthopaedics, Nemours/Alfred I. duPont Hospital for Children, Wilmington, Delaware, USA; Department of Orthopedics and Traumatology, Faculty of Medicine, Adnan Menderes University, Aydin, Turkey
2 Department of Orthopaedics, Nemours/Alfred I. duPont Hospital for Children, Wilmington, Delaware, USA

Date of Web Publication23-Jul-2019

Correspondence Address:
Dr. Suken A Shah
Department of Orthopaedics, Nemours/Alfred I. duPont Hospital for Children, 1600 Rockland Rd., Wilmington, DE 19803
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/isj.isj_36_18

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  Abstract 


Background: Spinal deformities are frequently seen in osteogenesis imperfecta (OI). We investigated contemporary spinal fusion techniques including pedicle screw fixation with or without cement augmentation in OI patients with scoliosis. Materials and Methods: OI patients with posterior-only scoliosis surgery were reviewed retrospectively (2005–2017). Preoperative and postoperative clinical status was compared. The radiographic review included pelvic obliquity, major curve magnitude, coronal balance, apical vertebral translation (AVT), lowest instrumented vertebrae (LIV) tilt angle, proximal and distal junctional angle, T1–S1 distance, and T1-pelvic angle. Results: Sixteen patients were included in the study. The mean age at surgery was 14 years (range, 6–19). The average follow-up period was 80 ± 40 months (range, 24–148). Mean preoperative curve magnitude of 76° ± 19° was significantly larger than the initial (31° ± 16°) and final (32° ± 17°) postoperative curve magnitudes (58% correction; P < 0.001). Mean preoperative AVT and LIV tilt angle were significantly higher than the initial and final postoperative measurements (P < 0.001 and P < 0.001, respectively). There was no difference between the measurements of coronal balance, pelvic obliquity, and T1–S1 distance among the preoperative, initial postoperative, and final follow-up measurements (P = 0.479, P= 0.125, and P= 0.05, respectively). There was no proximal junctional failure but one distal junctional failure led to revision surgery. Ambulatory status was unchanged in all patients, but an improvement in subjective self-reported clinical complaints was observed. Conclusion: Pedicle screw instrumentation with or without cement augmentation provided stability with few complications and improved clinical outcomes. Although preoperative activity level did not change compared with postoperative activity, there was an improvement in self-reported clinical complaints.

Keywords: Cement augmentation, osteogenesis imperfecta, scoliosis


How to cite this article:
Cobanoglu M, Bauer JM, Neiss G, Yorgova P, Rogers K, Kruse RW, Shah SA. Treatment of scoliosis in osteogenesis imperfecta: Experience at a single institution. Indian Spine J 2019;2:114-21

How to cite this URL:
Cobanoglu M, Bauer JM, Neiss G, Yorgova P, Rogers K, Kruse RW, Shah SA. Treatment of scoliosis in osteogenesis imperfecta: Experience at a single institution. Indian Spine J [serial online] 2019 [cited 2019 Oct 20];2:114-21. Available from: http://www.isjonline.com/text.asp?2019/2/2/114/263276




  Introduction Top


Osteogenesis imperfecta (OI) is a rare genetic connective tissue disorder, generally characterized by bone fragility, low bone mass, ligamentous laxity, short stature, and deformities of the extremities and spine caused by a qualitative or quantitative defect of type I collagen. OI is classically divided into four types (I, II, III, and IV), based on phenotypic expression according to Sillence et al.[1] This has been expanded to include OI type V, with calcification of the interosseous membrane,[2] and more recent research has found at least 17 different mutations that comprise these five types.[3] Spinal deformities, spondylolisthesis, and craniocervical junction problems are frequently seen in these patients.[4],[5] The prevalence of scoliosis in the OI population varies from 39% to 88%, depending on the age and severity of the disease.[6] Management of scoliosis is mandatory to prevent problems with self-care, mobility, pulmonary function, sitting balance, and interference with upper extremity function.[7]

Vertebral fractures due to the fragility of the bones and injury to the vertebral growth plate are thought to be a major cause of scoliosis in patients with OI.[8] Brace treatment was ineffective due to the fragility of the rib cage and existing chest wall deformity.[9],[10] The poor bone quality and rigidity of the deformity can also be challenging in the surgical treatment of scoliosis in OI, and the optimal technique remains to be determined.[11],[12] Currently, pedicle screws are the most commonly used instrumentation for scoliosis; however, osteoporotic bone as in OI may not allow satisfactory implant purchase to correct the deformity and to maintain stability. To enhance screw purchase, polymethylmethacrylate cement augmentation has been shown to reduce the risk of pullout.[13] This principle has been applied to cement-augmented pedicle screw fixation for scoliosis in OI.[7]

In this case series, we present a preliminary experience of treating scoliosis in OI at a single institution. The aim was to investigate whether pedicle screw fixation with and without cement augmentation successfully treated OI patients with scoliosis with regard to spinal stabilization, complications, and clinical outcomes.


  Materials and Methods Top


After Institutional Review Board approval, the records of OI patients with scoliosis who underwent posterior scoliosis surgery between 2005 and 2017 were reviewed retrospectively. Patients with <1 year of follow-up were excluded from the study. The type of OI was categorized according to the Sillence classification.[1] The patients who had a different genetic finding, inconsistent with Sillence classification, were defined as other. Patients' preoperative and postoperative activity level and changes in clinical complaints were recorded. Ambulatory status was evaluated according to the Bleck classification.[14] Preoperative bone densitometry data (dual-energy X-ray absorptiometry [DXA] on the Hologic Discovery DXA scanner, software version 12.3, Marlborough, MA USA) in the lumbar spine was recorded. If present, pulmonary compromise was recorded as a subjective self-reported clinical complaint. There was no pulmonary test available which needs to evaluate the pulmonary status of the patients before surgery in the patient's charts.

Surgical data

Surgical fusion data included the type of instrumentation, additional bony procedures (osteotomy, costotransversectomy), blood loss, number of cemented vertebrae, hospitalization period, and complications. There was no set protocol for which patients received the costotransversectomy to prevent pulmonary compromise postoperatively; clinical judgment was used in each case as to who to use this surgical technique in. In the cemented vertebra, nonfenestrated pedicle screws (DePuy Synthes Spine, Inc., Raynham, MA USA) were inserted after cement application (Confidence Spinal Cement System, DePuy Spine Inc.).

Radiographic data

Magnitude of pelvic obliquity, curve degree (Cobb angle), deviation in coronal balance, apical vertebral translation (AVT), lowest instrumented vertebrae (LIV) tilt angle, proximal and distal junctional angles, distance between T1 to S1, and T1-pelvic angle (TPA) were evaluated on preoperative, first postoperative, and final follow-up standing or sitting posteroanterior spine radiographs. Pelvic obliquity was measured as the angle between a line drawn perpendicular from the middle of T1 to S1 and the iliac crest line.[15],[16]

Statistical analysis

Because of the small sample size, nonparametric tests were used. The Friedman test was used to compare preoperative, first postoperative, and final follow-up radiographic data. Descriptive statistics were presented as mean ± standard deviation. When a difference existed between the measurements, a Wilcoxon test was applied as a post-hoc test to determine which group caused the difference. A valueof P < 0.05 was considered statistically significant. SPSS, version 22 (IBM, Inc., Armonk, NY, USA) was used for all statistical analysis. Correction rate in curve degree was calculated with the following formula:




  Results Top


There were 20 OI patients who underwent surgery for scoliosis. Sixteen of these patients met the inclusion criteria. The mean age at the time of surgery was 14 years (range, 6–19 years). The average follow-up period was 80 ± 40 months (range, 24–148 months). A chart including patient age, age at surgery and radiographic data are reported in [Table 1]. The distribution of the patients according to the type of OI was as follows: Sillence type I–two patients, III–10 patients, IV–three patients, and other (noncollagenous mutation)–one patient. Nine patients were wheelchair-bound preoperatively (level 0) and seven were ambulatory with or without support (levels 2–4), and the major preoperative complaint was back pain. Ambulatory status was not changed during follow-up in all patients, but improvement in clinical status was observed [Table 2]. All patients received intravenous pamidronate therapy preoperatively to increase bone mineral density. A 3-mg/kg cycle (1 mg/kg/day for 3 days) of pamidronate was given a week to a month before the surgery and after fusion mass/healing was complete. Thirteen patients resumed pamidronate infusions after surgery. The mean preoperative overall L1–L4 bone mineral density and Z-score were 0.568 g/cm2 (range, 0.282–0.835 g/cm2) and −2.8 (range, −6.7 to −1.0 g/cm2), respectively, in eight patients who had this data available. There were no data available for bone density for the other six patients. One patient had cervical spine surgery due to basilar impression before the scoliosis surgery.
Table 1: Demographic characteristics and radiographic data

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Table 2: Preoperative and postoperative activity level and clinical status

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Surgical data

A 6-year-old ambulatory patient was treated with magnetically-controlled growing rods (MCGR) with pedicle screw fixation without cement augmentation. The others underwent spinal fusion with pedicle screw instrumentation [Figure 1]. One patient had hook instrumentation in addition to pedicle screw at the proximal anchors. Ten patients had cement-augmented pedicle screw insertion at the proximal and distal foundations [mean augmented screws: five, range three to seven; [Figure 2]. Although no implant-related complications had been encountered in the first three cases, the cement-augmented screw began to be used after these first three cases to increase the purchase of the screws, except in the patient treated with MCGR. No complications related to cement augmentation were observed during surgery. Six patients had costotransversectomy to correct deformity arising from rib deformity and to gain more flexibility at the apex of the curves. Three of these 6 patients needed ventilator support in the intensive care unit. Halo traction was applied during two surgeries. One patient had two-stage operation including the first stage with halo traction application for 10 days and the second stage with posterior fusion. The patient characteristics for these surgical step variations are included in [Table 3]. The mean estimated blood loss was 2068 ± 1188 cc (range, 300–4500 cc) and mean hospitalization time was 7 ± 4 days (range, 4–19 days). In the early postoperative period, two patients had superficial wound drainage that resolved with oral antibiotic treatment and dressing. Although there was no implant complication during index surgery, the patient treated with MCGR presented with distal junctional failure (L2 distal screw failure, not initially cemented) one month after index surgery and it was treated with reinsertion of spinal instrumentation and vertebroplasty with cement-augmented pedicle screw fixation. One patient suffered from transient ulnar nerve palsy due to positioning during operation; this was detected intraoperatively by upper extremity somatosensory evoked potentials and was completely resolved by 6 weeks after surgery. There were no nerve root or spinal cord deficits during the surgeries. No other postoperative complication was observed during the follow-up period. There was no other instrumentation failure at the latest follow-up.
Figure 1: (a) Preoperative clinical view of the patient from posterior and lateral aspect, (b) Preoperative sitting posteroanterior and lateral spine radiographs show severe scoliosis (96°) and thoracic hypokyphosis (11°). (c) Initial postoperative sitting posteroanterior and lateral spine radiographs show correction of the scoliosis (35°) and kyphosis (24°) with pedicle screw fixation with cement augmentation. (d) Postoperative 4-year follow-up sitting posteroanterior and lateral spine radiographs show no implant failure nor correction loss (scoliosis 34°, kyphosis 23°)

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Figure 2: (a) Cement injection into the vertebral body under fluoroscopic monitoring, which was then followed by screw placement. (b) Lateral view. (c) Posteroanterior view

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Table 3: Characteristics of the patients according to the surgical step variations (values are mean±standard deviation)

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Radiographic data

The mean preoperative Cobb angle 76° ± 19° was significantly more severe than both the initial postoperative (31° ± 16°) and final follow-up (32° ± 17°) Cobb angles (58% correction; P < 0.001). There was no difference between the first postoperative and the last follow-up Cobb angle (P = 0.146). No correction loss was found during the follow-up [Table 4]. Only one patient who treated with MCGR had 17° of improvement in curve magnitude at the first and last postoperative follow-up.
Table 4: Comparison of radiographic data (values are mean±standard deviation)

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The mean preoperative AVT (67 ± 24 mm) was significantly higher than those at the initial postoperative (30 ± 15 mm) and last follow-up (32 ± 17 mm) (P < 0.001). There was no statistically significant difference between initial and final postoperative AVT. This was a little increase not leading to significant difference and statistically significant incompatibility with the results between initial postoperative and final follow-up Cobb angle (P = 0.089) [Table 4].

The mean preoperative LIV tilt (21° ± 8°) was significantly higher than those at the initial postoperative (7° ± 5°) and last follow-up (6° ± 6°) (P < 0.001). There was no statistically significant difference between the initial and final postoperative LIV tilt (P = 0.304) [Table 4].

There was no statistically significant difference in the measurements of coronal balance, pelvic obliquity, and T1–S1 distance among the preoperative, first postoperative, and last follow-up measurements [P = 0.479, P = 0.125, and P = 0.05, respectively; [Table 4]. The measurement of coronal balance can be effected by patient position on X-ray, little errors of selecting points on measuring on X-rays. Because of these possible reasons, there may not be seen a significant difference in change in coronal balance as much as seen in the curve magnitude.

Poor visualization of the lateral spinal plane in these patients precluded measurements of the sagittal spine parameters including thoracic kyphosis, lumbar lordosis, proximal-distal junctional kyphosis, and TPA in each patient. For this reason, they could not be measured on each lateral radiograph. The mean proximal junctional angle on the first and last follow-up upright lateral radiographs were 0° ± 11° (n = 10; range, −14° to 19°) and 0° ± 9.6° (n = 7; range −15° to 17°), respectively. The mean distal junctional angle on the first and last follow-up upright lateral radiographs were −23° ± 24.5° (n = 12, range, −55° to 2°), and −28° ± 18.7° (n = 11; range, −56° to 0). No patient underwent revision surgery due to proximal junctional failure. The mean preoperative and postoperative TPAs were 12° ± 20° (n = 4; range, −4° to 46°) and 17° ± 11° (n = 4; range, 5° to 30°), respectively.


  Discussion Top


Scoliosis is frequently seen in OI and can lead to pain and decrease in functional status and respiratory capacity, which is the major cause of death in severe forms of OI.[17],[18] The population in this study included different types of OI patients (nonambulatory and ambulatory) with different phenotypic and genetic mutation classes (Collagen Type I Alpha 1 or Collagen Type I Alpha 2[19] and Non-Collagen 1). However, regardless of OI type, current indications for fusion are curves above 50° in patients who are past peak height velocity or in the presence of substantial curve progression after skeletal maturity because these curves can continue to progress in adulthood.[7],[10] In this case series, the surgical indication included a Cobb angle above 50°. In the surgical approach, the first consideration is the potential challenge in surgical exposure to access the posterior spinal elements due to the severity of rib cage deformity.[10] The other important issue is to achieve stable fixation in the OI spine, which has been technically demanding due to implant failure in poor bone quality, as seen in the elderly osteoporotic population.[13]

Historically, there have been several strategies for surgical fusion in the treatment of OI with scoliosis.[7],[9],[12],[20],[21] Early studies emphasized stabilization with minimal to no attempt at curve correction.[20],[22] This resulted in excellent fusion rates, 100% and 93%, respectively, by a combination of noninstrumented, Harrington, and Luque constructs. Yong-Hing and MacEwen achieved 36% Cobb correction in a 60-patient cohort, with a 7% better correction in those treated with Harrington rods compared with the noninstrumented group. This early instrumentation, however, contributed to a >50% incidence of complications, which was also related to preoperative curve and kyphosis magnitude.[23] Benson and Newman recommended improving on the Harrington construct by supplementing the hooks with methyl methacrylate bone cement, which decreased postoperative Cobb progression by 50% in their small cohort of three patients without instrumentation and nine with instrumentation.[9] Another advancement came with preoperative halo traction followed by in situ fusion, with Cotrel–Dubousset instrumentation (18 patients) and Harrington instrumentation (two patients). The authors achieved 32% Cobb improvement with traction, which reduced to 25% after fusion in long-term follow-up.[12] However, average halo duration was 90 days and several complications occurred, all in OI type III patients: two intraoperative lamina fractures requiring adjacent level hooks, three failures of instrumentation, and one pseudarthrosis and rod breakage. This was the only study to report improved ambulation level, which occurred in 35% of patients. Our study did not find this improvement, which was in keeping with others.[21],[22]

This is the first single-institution study to report cement-augmented pedicle screw fixation in OI scoliosis surgery, and the largest reported cohort for both this technique as well as modern pedicle screw fixation in OI. Yilmaz et al. reviewed a 10-patient series from two institutions who were treated with posterior spinal fusion for scoliosis. Seven patients had cement-augmented pedicle screw instrumentation at the proximal and distal anchors to prevent pull-out. These authors were the first to report this technique, which is used here and includes a portion of this cohort; they also first reported the difficulty in the exposure of the thoracic region. The authors reported average correction of 48% with no loss of correction at follow-up without neurologic deficits and implant failures.[7] Our case series showed an improvement in the Cobb correction (58% correction), the AVT, and the LIV tilt. Both studies' correction was maintained during the follow-up period and represent an improvement over the past techniques' reported correction of 32%–36%.[12],[23] In this cohort, there was one implant-related complication in one case (Type I) with distal screw failure at 1 month treated with cement-augmentation revision. There were no other implant-related complications in this case series at the time of final follow-up, demonstrating a large improvement over less modern instrumentation. Although historical methods of fusion have not been found to improve lung volumes, these modern techniques may improve results, and fusion can prevent progressive respiratory decline resulting from thoracic insufficiency syndrome.[4]

In all patients, pamidronate had been administered for several years before surgery to improve bone quality and decrease the rate of fractures,[24] which should improve pedicle screw purchase.[25] The goal of this medication is to both improve bone quality for screw purchase and to also decrease bone turnover with the idea that it may minimize osteoclastic resorption around the screw. We are approaching this as a medical adjunct to surgery and general bisphosphonate treatment can be resumed with specific patient indications following the second cycle. An inverse correlation has been reported between the extent of scoliotic curvature and the Z-score bone mineral density of the lumbar spine, as well as the thoracic kyphosis angle.[8] The mean preoperative overall L1–L4 bone mineral density and Z-score were 0.568 g/cm2 (range, 0.282–0.835 g/cm2) and −2.8 g/cm2 (range, −6.7 to −1 g/cm2). Cement augmentation was performed to the distal end of the instrumentation to increase the purchase of the pedicle screws to reduce the risk of pull out at the most proximal and distal end of the construct where most of the load is applied and potential implant failure may occur.

In this study, limitations included small cohort size, the absence of pulmonary function tests, and validated questionnaire for the comparison between preoperative and postoperative status. We could not evaluate the fusion of the spine by computed tomography. The small cohort size prevented direct comparison between patients treated with and without augmentation. It was also a retrospective study without a treatment protocol, with augmentation chosen by surgeon preference, thus there was a bias to use it in the patients with worse bone. There was also no set protocol for which patients received costotransversectomy or halo traction. Although this study is the extension of a previous study that included cases from two different institutions,[7] this study evaluated a larger group of patients with a relatively long-term followup from a single institution and detailed information about the surgery.


  Conclusion Top


This case series included the patients with long-term follow-up and demonstrated the reliability of this surgical technique with the pedicle screw system. We believe that cement augmentation may reduce the screw pull out in OI patients with scoliosis. Although preoperative activity level did not change compared with postoperative activity, an improvement in subjective clinical complaints was observed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Bonafe L, Cormier-Daire V, Hall C, Lachman R, Mortier G, Mundlos S, et al. Nosology and classification of genetic skeletal disorders: 2015 revision. Am J Med Genet A 2015;167A:2869-92.  Back to cited text no. 3
    
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Widmann RF, Bitan FD, Laplaza FJ, Burke SW, DiMaio MF, Schneider R, et al. Spinal deformity, pulmonary compromise, and quality of life in osteogenesis imperfecta. Spine (Phila Pa 1976) 1999;24:1673-8.  Back to cited text no. 4
    
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Engelbert RH, Gerver WJ, Breslau-Siderius LJ, van der Graaf Y, Pruijs HE, van Doorne JM, et al. Spinal complications in osteogenesis imperfecta: 47 patients 1-16 years of age. Acta Orthop Scand 1998;69:283-6.  Back to cited text no. 5
    
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Yilmaz G, Hwang S, Oto M, Kruse R, Rogers KJ, Bober MB, et al. Surgical treatment of scoliosis in osteogenesis imperfecta with cement-augmented pedicle screw instrumentation. J Spinal Disord Tech 2014;27:174-80.  Back to cited text no. 7
    
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Wallace MJ, Kruse RW, Shah SA. The spine in patients with osteogenesis imperfecta. J Am Acad Orthop Surg 2017;25:100-9.  Back to cited text no. 10
    
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12.
Janus GJ, Finidori G, Engelbert RH, Pouliquen M, Pruijs JE. Operative treatment of severe scoliosis in osteogenesis imperfecta: Results of 20 patients after halo traction and posterior spondylodesis with instrumentation. Eur Spine J 2000;9:486-91.  Back to cited text no. 12
    
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Leichtle CI, Lorenz A, Rothstock S, Happel J, Walter F, Shiozawa T, et al. Pull-out strength of cemented solid versus fenestrated pedicle screws in osteoporotic vertebrae. Bone Joint Res 2016;5:419-26.  Back to cited text no. 13
    
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Bleck EE. Nonoperative treatment of osteogenesis imperfecta: Orthotic and mobility management. Clin Orthop Relat Res 1981;158:111-22.  Back to cited text no. 14
    
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Dayer R, Ouellet JA, Saran N. Pelvic fixation for neuromuscular scoliosis deformity correction. Curr Rev Musculoskelet Med 2012;5:91-101.  Back to cited text no. 15
    
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Sato A, Ouellet J, Muneta T, Glorieux FH, Rauch F. Scoliosis in osteogenesis imperfecta caused by COL1A1/COL1A2 mutations – Genotype-phenotype correlations and effect of bisphosphonate treatment. Bone 2016;86:53-7.  Back to cited text no. 19
    
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24.
Rauch F, Travers R, Plotkin H, Glorieux FH. The effects of intravenous pamidronate on the bone tissue of children and adolescents with osteogenesis imperfecta. J Clin Invest 2002;110:1293-9.  Back to cited text no. 24
    
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Halvorson TL, Kelley LA, Thomas KA, Whitecloud TS 3rd, Cook SD. Effects of bone mineral density on pedicle screw fixation. Spine (Phila Pa 1976) 1994;19:2415-20.  Back to cited text no. 25
    


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