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Jurnal Skoliosis
Jurnal Skoliosis
Management and outcomes of scoliosis in children with congenital diaphrag-
matic hernia
PII: S0022-3468(16)30336-0
DOI: doi: 10.1016/j.jpedsurg.2016.09.013
Reference: YJPSU 57782
Please cite this article as: Antiel Ryan M., Riley John S., Cahill Patrick J., Campbell
Robert M., Waqar Lindsay, Herkert Lisa M., Rintoul Natalie E., Peranteau William H.,
Flake Alan W., Adzick N. Scott, Hedrick Holly L., Management and outcomes of scoliosis
in children with congenital diaphragmatic hernia, Journal of Pediatric Surgery (2016), doi:
10.1016/j.jpedsurg.2016.09.013
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Ryan M. Antiel, John S. Riley, Patrick J. Cahill, Robert M. Campbell, Lindsay Waqar,
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Lisa M. Herkert, Natalie E. Rintoul William H. Peranteau, Alan W. Flake, N. Scott
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The Center for Fetal Diagnosis and Treatment, Center for Thoracic Insufficiency
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Syndrome, and the Division of Orthopedics, The Children’s Hospital of Philadelphia,
Philadelphia, PA 19104-4318
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Abstract
Purpose: The purpose of this study was to evaluate the management and outcomes of
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Methods: From January 1996 to August 2015, 26 of 380 (7%) CDH patients were
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diagnosed with scoliosis. Six (23%) were prenatally diagnosed by ultrasound, and 9
(35%) were diagnosed postnatally. The remaining 11 (42%) developed scoliosis after
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discharge. Mean follow-up was 6.6 years.
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Results: Among the 15 patients with congenital scoliosis, there were 2 (13%) perinatal
deaths. Five of the 13 (38%) survivors required orthopedic surgery, and 2 have required
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bracing. The mean age at initial surgery was 7 years. These five children underwent an
average of 2.8 (range 1-7) expansions or revisions. All surgical patients required
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patients who developed scoliosis later in life required surgery, but 3 have required
bracing. Six of the 11 (55%) required a patch repair for CDH compared to 158 of 264
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Conclusions: Early diagnosis of scoliosis in CDH patients is associated with a high rate
of surgery. There was not a higher incidence of patch repair among patients who
developed scoliosis.
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Introduction
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approximately 1 in every 3000 live births. [1] The incomplete formation of the diaphragm
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musculature during development allows the abdominal viscera to migrate into the
thoracic cavity. [2] Compression of the developing fetal lungs causes pulmonary
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hypoplasia and pulmonary hypertension, which results in a high mortality rate, estimated
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between 20-60%. [3-4] Small diaphragmatic defects can be repaired by primary closure
while larger defects require repair with a synthetic patch or autologous muscle flap.
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Survivors with CDH can have multiple comorbidities including respiratory insufficiency,
degrees, scoliosis can occur in CDH patients before birth (congenital scoliosis) or
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develop later in childhood. The purpose of this study was two-fold: first, to describe the
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prevalence of scoliosis in a large cohort of CDH patients; and, second, to evaluate the
Methods
Review Board.
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Study population
We reviewed 380 patients with CDH who are part of the Pulmonary Hypoplasia
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Program Database at the Children’s Hospital of Philadelphia from January 1996 through
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August 2015. Many of these patients underwent prenatal evaluation at our Center for
Fetal Diagnosis and Treatment, which included a fetal ultrasound and magnetic resonance
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imaging. All CDH patients with a diagnosis of scoliosis from the Pulmonary Hypoplasia
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Program database or Orthopedic scoliosis database were included in this study. Patients
were categorized by the timing of scoliosis diagnosis: prenatal, postnatal diagnosis during
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the neonatal hospitalization, or sometime after hospital discharge. Prenatal records were
reviewed to determine demographics, CDH side (right vs. left), liver position (above or
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below the diaphragm), and presence of other genetic abnormalities. Postnatal records
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were reviewed for survival, gestational age at birth, birth weight, timing of CDH repair,
Orthopedic evaluation
We reviewed orthopedic records to determine need for bracing, need and timing
of orthopedic surgery, type of repair (growing rod, spinal fusion, or vertical expandable
to determine which patients had prenatal diagnosis of scoliosis. Optimal imaging of the
spine required positioning the fetal spine in the near field and away from the uterine wall.
[6] Coronal views of the spine were best for identifying the location of curvature. The
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direction was indicated by stating the side to which the convex portion of the spine
pointed. The approximate level of the center of the curvature was noted. The Cobb angle
was measured from coronal images using the same principles used when measuring from
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a radiograph, however the severity was usually described qualitatively.
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Preoperative and postoperative upright anteroposterior spine and chest
radiographs were reviewed for all patients who underwent orthopedic surgery, as was the
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most recently obtained x-ray for all patients, in order to determine the Cobb angle and to
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assess space available for lung (SAL). X-rays were performed in standing (children and
apex of the curve of the spine.[7-8] A line was drawn along the superior end plate of the
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top vertebra and a second line was drawn along the inferior end plate of the bottom
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vertebra. The angle between these two intersecting lines was designated as the Cobb
angle. The SAL was calculated as a ratio, expressed as a percentage, by dividing the
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height of the concave hemithorax by the height of the convex hemithorax.[9] The height
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of the hemithorax was measured by taking the distance from the middle of the most
cephalad rib down to the center of the hemidiaphragm. Cobb angles were measured and
recorded by the orthopedic investigators (P.J.C. and R.M.C.) and the SAL was calculated
Statistical analysis
percentage, and continuous variables were reported as mean and standard deviation or
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median and interquartile range. Categorical variables were compared between CDH
patients with and without scoliosis using the Chi square test. Pre and post-operative
continuous variables were compared using a paired Student’s t-test. All statistical tests
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were two-sided with the α level set at 0.05 for statistical significance. Statistical analysis
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was performed using Stata statistical software, version 13.1 (StataCorp, College Station,
TX).
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Results
Patient population
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From January 1996 to August 2015, a total of 26 of 380 (7%) CDH patients were
diagnosed with scoliosis. Fifteen patients (58%) had congenital scoliosis. Six (40%)
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were diagnosed prenatally by ultrasound and 9 (60%) were diagnosed postnatally during
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(20%) had abnormal karyotypes and there were 2 (13%) perinatal deaths of neonates with
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(4%) patients were diagnosed with scoliosis later in life, sometime after their neonatal
hospital discharge. There have been no deaths among the patients who developed
scoliosis later in life. The incidence of scoliosis among survivors at NICU discharge was
24/274 (9%). Patient characteristics and neonatal hospital course are summarized in
The mean gestational age at delivery was 36.6 weeks (SD 2.9 weeks). Of the 24
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(32%) a curve convex away from the diaphragmatic defect. The average timing of hernia
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repair was 11 days (SD 12 days). Thirteen of the 24 patients (54%) required a prosthetic
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patch for the repair of their diaphragm. Six of the 11 (55%) who developed scoliosis
later in life had required a patch repair for CDH compared to 158 of 264 (60%) of all
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CDH survivors at NICU discharge without scoliosis during the study period (p=0.73).
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Musculoskeletal and pulmonary outcomes
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Five of the 13(38%) survivors with congenital scoliosis required orthopedic surgery and 2
have required bracing. There were 3 VEPTR placements, 1 growing rod placement, and
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1 spinal fusion. The mean age at initial surgery was 7 years. These five children
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underwent an average of 2.8 (range 1-7) expansions or revisions. The mean pre-
operative Cobb angle was 50° (range 21-69) reducing to a post-operative mean of 31°
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(range 11-47, p=0.01) and then increasing to a mean of 47° (range 11-65, p=0.55) at time
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of maximal follow-up. The average time between preoperative imaging and most recent
imaging was 30.8 months. The mean pre-operative space available for lung was 90%
(range 81-96) increasing to a post-operative mean of 95% (range 85-99) and a mean of
95% (range 92-99) at maximal follow-up (p=0.24). These results are consistent with
other reported results of early onset scoliosis. [10] The scoliosis initially improves
following surgery yet worsens over time until the patient requires an expansion or
revision. All surgical patients required supplemental oxygen at 30 days of life for
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None of the 11 patients who developed scoliosis later in life required orthopedic
surgery to date, however 3 have required bracing. The mean Cobb angle of brace treated
patients was 32° (range 7-58) compared to a mean of 12° (range 0-34) for patients being
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observed. The mean space available for lung was 88% (range 83-98) and 92% (range 83-
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100), respectively.
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Discussion
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Although advances in surgical and neonatal care have led to significantly
improved overall survival rates for neonates with CDH, long-term survivors face
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numerous morbidities including musculoskeletal deformities.[5] Patients with CDH
suffer from underlying pulmonary hypoplasia and pulmonary hypertension. Scoliosis can
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syndrome.[9, 11-12] In this retrospective review of 380 patients with CDH over twenty
years, the incidence of scoliosis was 7% (9% among survivors at NICU discharge). This
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follow-up times and later deaths. Of the CDH patients diagnosed with scoliosis prior to
NICU discharge, just over half (58%) were diagnosed with congenital scoliosis and a
Thirty-eight percent of the CDH patients diagnosed with congenital scoliosis required
orthopedic surgery, whereas none of the patients in our cohort who have developed
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than 10 degrees in the coronal plane, is approximately 3%.[13-14] Infants who have
undergone thoracic surgery for congenital heart defects, esophageal atresia, and rib or
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chest wall resection have a higher than expected incidence of scoliosis in
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adolescence.[15-18] Patients with CDH also have a significantly higher rate of
scoliosis.[19] Most recent series report rates ranging from 8% - 27%.[20-22] Ours is the
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first study that describes the rate of prenatal diagnosis as well as the orthopedic
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management and outcomes of all patients with CDH and scoliosis.
For patients with a curvature less than 20 degrees, careful monitoring with serial
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radiographic exams is sufficient. For patients with curvature between 20 and 40 degrees,
back bracing can be an effective nonsurgical treatment. For children with a curvature
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greater than 40 degrees and for those with thoracic insufficiency syndrome, surgical
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management is warranted. Of the surgical treatments for scoliosis, growing rods have
been the most common treatment for children who have not reached skeletal maturity,
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whereas spinal fusion is the most common surgical treatment for children who have
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reached skeletal maturity. More recently vertical expandable prosthetic titanium ribs
(VEPTR) has become the preferred treatment for patients who suffer from thoracic
which the devise is attached to the top and base of the spine, VEPTR is also attached to
the patient’s ribs. This not only straightens the spine but also separates the ribs resulting
in better lung growth and pulmonary function. VEPTR and growing rods require
adjustment surgeries every 6-8 months until the child reaches skeletal maturity.
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While the association between CDH and scoliosis is well established, the etiology
still remains unclear. Although the etiology is likely multifactorial, there are at least two
general ways to think about this association. First, congenital scoliosis is due to
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structural abnormalities of the spine and primarily associated with CDH given the close
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embryological relationship between the development of the lungs, diaphragm, and
thoracic spine. However, as indicated by our data, a significant minority of CDH patients
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will develop scoliosis later in life. Second, scoliosis as a secondary development is
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hypothesized to be associated with restricted growth of the hemithorax secondary to
pectus malformations among patients who have required patch repair, the current data
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does not support an association between patch repair and scoliosis.[26] There was not a
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statistically significant difference in requirement for patch repair among patients who
developed scoliosis compared to those who did not develop scoliosis (55 vs. 60 %,
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p=0.73).
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Our study has important limitations. First, the incidence of scoliosis was
remains unknown. The published incidence of hemivertebra in the fetus is 0.33 in 1000
births. [27] However, only 25% of fetuses diagnosed with hemivertebra have associated
scoliosis/kyphosis. [28]. We are the first group, to our knowledge, to publish on the
antenatal diagnosis of scoliosis in CDH patients. It is possible that very mild scoliosis
was not identified on prenatal ultrasound or during the neonatal hospitalization. It is also
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probable that there were patients who developed mild scoliosis later in life that either
went undetected or who have been lost to follow-up. Therefore, our total incidence rate
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patients. This study does not propose a specific mechanism for the development of
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scoliosis in CDH; rather we sought to report the incidence, management, and outcomes in
our practice. Nonetheless, the type of surgical repair did not affect the incidence of
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scoliosis. This finding challenges the hypothesis that the tension after repair leads to the
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development of scoliosis.[29]
recommend that all anatomic surveys for fetuses with CDH include a complete evaluation
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of the spine. Early diagnosis is associated with a relatively high rate of surgery and
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bracing, whereas late diagnosis appears to be associated with relatively mild scoliosis.
Among CDH patients who are diagnosed prenatally or in the neonatal hospitalization
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with congenital scoliosis, there was a 13% mortality rate and 38% of survivors with
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congenital scoliosis have required orthopedic surgery. In contrast, none of the patients
who have developed scoliosis later in life have required orthopedic surgery to date.
These data support careful musculoskeletal monitoring of CDH patients and early
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References
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6. Coleman BG, Langer JE, Horii SC. The diagnostic features of spina bifida: the
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9. Campbell RM Jr, Smith MD, Mayes TC, et al. The characteristics of thoracic
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insufficiency syndrome associated with fused ribs and congenital scoliosis. J
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Bone Joint Surg Am. 2003;85(3):399-408.
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technique for pediatric congenital spinal deformities. J Pediatr Orthop.
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11. Campbell RM Jr, Hell-Vocke AK. Growth of the thoracic spine in congenital
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scoliosis after expansion thoracoplasty. J Bone Joint Surg Am 2003; 85:409–420
asymmetry in children with congenital and infantile scoliosis. The Spine Journal
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2008; 8:639–644
13. Reamy BV1, Slakey JB. Adolescent idiopathic scoliosis: review and current
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14. Roach JW. Adolescent idiopathic scoliosis. Orthop Clin North Am. 1999; 30:353.
15. Farley FA, Phillips WA, Herzenberg JE, et al. Natural history of scoliosis in
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thoracotomy for esophageal atresia. Report of a case and review of the literature.
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18. Glotzbecker MP, Gold M, Puder M, Hresko MT. Scoliosis after chest wall
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resection. J Child Orthop. 2013; 7: 301–307.
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deformities preventable? Pediatr Surg Int 2011; 27:1343–9.
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20. Russell KW, Barnhart DC, Rollins MD, Hedlund G, Scaife ER. Musculoskeletal
22. Vanamo K, Peltonen J, Rintala R, et al. Chest wall and spinal deformities in
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23. Campbell RM Jr, Smith MD, Mayes TC et al. The effect of opening wedge
24. Campbell RM Jr, Smith MD, Hell-Vocke AK. Expansion thoracoplasty: the
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25. Hell AK, Campbell RM, Hefti F. The vertical expandable prosthetic titanium rib
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14:287–293.
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26. Tsai J, Sulkowski J, Adzick NS, Hedrick HL, Flake AW. Patch repair for
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47:637-41.
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27. Goldstein I, Makhoul IR,Weissman A, Drugan A. Hemivertebra: prenatal
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28. Basude S, et al. Fetal hemivertebra: associations and perinatal outcome.
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Figure Legends:
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A. Pre-surgical chest radiograph with Cobb angel 69.1 and SAL 96%.
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B. Post-surgical chest radiograph with Cobb angel 55.1 and SAL 99%.
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Fig. 1A
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Fig. 1B
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Demographics
Female sex 10 (38%) 5 (33%) 5 (45%) 0.53
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Race 0.90
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White 18 (69%) 10 (66%) 8 (73%)
Black 4 (15%) 3 (20%) 1 (9%)
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Asian 2 (8%) 1 (7%) 1 (9%)
Other 2 (8%) 1 (7%) 1 (9%)
Perinatal information
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Side 1.0
LCDH 18 (69%) 10 (66%) 8 (73%)
RCDH 7 (27%) 4 (27%) 3 (27%)
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Midline defect 1 (4%) 1 (7%) 0
Liver up 13 (50%) 6 (39%) 7 (64%) 0.43
Normal karyotype 20 (77%) 12 (80%) 8 (73%) 1.0
Survival 24 (92%) 13 (87%) 11 (100%) 0.49
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Orthopedic interventions
VEPTR 3 (13%) 3 (23%) 0 -
Growing rod 1 (4%) 1 (8%) 0 -
Spinal fusion 1 (4%) 1 (8%) 0 -
Bracing 4 (17%) 1 (8%) 3 (27%) 0.28
Age at surgery 7 (3.27) 7 (3.27) - -
Mean (SD), years
Number of - 2.8 (1-7) - -
operations (range)
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Table 2: Cobb angles and space available for lung (SAL) of 24 CDH patients with
scoliosis
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Pre-surgical X-ray Post-surgical X-ray Most Recent Follow-up X-ray
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Cobb angle SAL Cobb SAL Cobb SAL
mean (range) mean (range) angle mean angle mean
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mean (range) mean (range)
(range) (range)
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Surgical 50° (21-69) 90% (81-96) 31° (11- 95% 44° (11- 95%
treatment 47) (85-99) 65) (92-99)
(n = 5)
Bracing - - - - 32° (7- 88%
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(n = 5) 58) (83-98)
Observation - - - - 12° (0- 92%
alone@ 34) (83-
(n = 14) 100)
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