The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 89, Issue 12

Scientific Articles | December 01, 2007

Natural History of Thoracic Insufficiency Syndrome: A Spondylothoracic Dysplasia Perspective

Norman Ramírez, MD¹; Alberto S. Cornier, MD, PhD²; Robert M. CampbellJr., MD³; Simón Carlo, MD²; Sandra Arroyo, MD⁴; Jesse Romeu, MD⁵

¹ Pediatric Orthopaedic Department, Hospital de la Concepción, P.O. Box 6847, Mayaguez, Puerto Rico 00681. E-mail address: normanpipe@aol.com
² Genetic Department, San Juan Bautista School of Medicine, Caguas, Puerto Rico 00725. E-mail address for A.S. Cornier: scornier@sanjuanbautista.edu. E-mail address for S. Carlo: scarlo@psm.edu
³ Thoracic Institute, Christus Santa Rosa Children's Hospital, 333 North Santa Rosa Street, San Antonio TX 78207. E-mail address: rcampbell.thoracic.institute@christushealth.org
⁴ BioImagenes Medicas, P.O. Box 876, Mayaguez, Puerto Rico 00681. E-mail address: saf@bioimagenesmedicas.com
⁵ CPR Professional Building, 55 Calle de Diego E, Suite 401, Mayaguez, Puerto Rico 00681

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Disclosure: The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

Investigation performed at Ponce Medical School and Hospital de la Concepción, San Germán, Puerto Rico

The Journal of Bone and Joint Surgery, Inc.

J Bone Joint Surg Am, 2007 Dec 01;89(12):2663-2675. doi: 10.2106/JBJS.F.01085

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Abstract

Background: Spondylothoracic dysplasia is a condition in which bilateral chest wall deformity due to costovertebral rib fusion with shortening of the thoracic spine results in severe thoracic insufficiency syndrome and early death. Little is known about the long-term respiratory natural history of this disorder and the specific anatomic deformity.

Methods: We conducted a multicenter prospective and retrospective study of patients with spondylothoracic dysplasia. Medical evaluations, respiratory history, physical examination findings, radiographs, computed tomographic scans, and pulmonary function tests were studied. Anatomic, radiographic, and functional parameters for the disorder were established to determine the natural history of the thoracic insufficiency syndrome.

Results: Twenty-eight patients were identified. Eight patients had died in the neonatal period, and twenty were evaluated (eleven prospectively and nine retrospectively). The survivors were doing well clinically, but the average spirometric values were 27.9% of the predicted normal value for the forced vital capacity (FVC), 29.5% of the predicted normal value for the forced expiratory volume in the first second (FEV1), and 0.92 for the FEV1/FVC ratio, demonstrating a severe restrictive respiratory pattern. The computed tomographic scan lung volumes were an average of 28% of the expected values for age and gender. The thorax was stiff from rib fusion and was severely shortened posteriorly, averaging 24.2% of the predicted normal length. The thoracic spine was predominantly composed of block vertebrae, whereas in the lumbar region there were multiple hemivertebrae. Minimal scoliosis was seen, and there were no neurological deficits.

Conclusions: Spondylothoracic dysplasia has a unique pathoanatomy of volume depletion deformity of the thorax with chest wall stiffness, resulting in thoracic insufficiency syndrome. Clinical tolerance of the restrictive lung disease in this disorder is impressive, but no clear reason has yet been identified for the clinical pulmonary health in the face of severe restrictive lung disease. Patients who survive infancy show no progression of congenital anomalies and can have a good quality of life. This disease may serve as a model of the natural history of thoracic insufficiency syndrome due to growth inhibition of the thoracic spine either as a result of congenital causes or secondary to surgical fusion early in life.

Level of Evidence: Prognostic Level IV. See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article

Introduction

Spondylothoracic dysplasia is an inherited condition of extreme extrinsic restrictive lung disease due to deformity of the thorax as a result of posterior rib fusion and severe shortening of the thoracic spine. The condition represents a severe volume-depletion deformity of the thorax through the reduction in height with a direct adverse effect on the growth of the underlying lungs resulting in severe thoracic insufficiency syndrome, which is defined as the inability of the thorax to support normal respiration or lung growth^1,2. This syndrome can present when there is congenital scoliosis with associated concave hemithorax rib fusion, which directly impairs unilateral thoracic volume, function, and growth, resulting in indirect limitation of lung growth and function². In patients with spondylothoracic dysplasia, the thoracic malformation is global, with bilateral congenital rib constriction. The anatomic defect of thoracic spine shortening associated with spondylothoracic dysplasia has some relevance as a natural history analog of the thoracic spinal shortening due to early spine fusion for the treatment of early-onset scoliosis. Little is known about the long-term clinical respiratory natural history of spondylothoracic dysplasia and the specific anatomic spine, rib cage, and diaphragmatic deformity.

In 1966, Lavy et al.³ described an autosomal recessive type of short trunk dwarfism with vertebral and rib anomalies. The patients had a markedly shortened thoracic spine and rib cage characterized by the partial absence of vertebral bodies as well as the presence of hemivertebrae and block vertebrae. In addition, all of the ribs were tightly fused at the costovertebral junction, flaring anteriorly and laterally. A unique radiographic "fan-like" appearance of the chest with the ribs radiating from this common articulation³ was described. In 1969, Moseley and Bonforte⁴ proposed the term spondylothoracic dysplasia to describe the same group of patients. Later, Pérez-Comas and García-Castro⁵ grouped patients with spondylothoracic dysplasia together with a larger population of patients with spinal segmentation, formation defects, and rib fusion anomalies under a general grouping termed Jarcho-Levin syndrome^6-19.

Because of the phenotypical and nosological inconsistencies between patients with spondylothoracic dysplasia and those presented by Jarcho and Levin⁶, Solomon et al.²⁰, in 1978, proposed the division of Jarcho-Levin syndrome into two groups: spondylocostal dysostosis and spondylothoracic dysplasia. Solomon et al. used the term spondylocostal dysostosis for patients with intrinsic rib changes such as broadening, bifurcation, and fusion associated with congenital scoliosis without the fan-like configuration of the thorax. Both autosomal dominant and recessive modes of inheritance have been described. While early deaths resulting from respiratory causes have been reported in association with spondylocostal dysostosis^{6,9,11,13,15,21}, Solomon et al. reported a better survival rate and overall prognosis when patients with spondylocostal dysostosis were compared with patients with spondylothoracic dysplasia²⁰. In contrast, the diagnosis of spondylothoracic dysplasia was suggested for patients with autosomal recessive inheritance and a fan-like configuration of the ribs resulting from the fusion at the costovertebral junction without intrinsic costal anomalies²⁰. All patients with spondylothoracic dysplasia in the study by Solomon et al. died early in life as a result of pulmonary complications²⁰.

The primary purpose of the present study was to characterize in detail the clinical respiratory status and physical examination features as well as the thoracic abnormalities of patients with spondylothoracic dysplasia from a thoracic insufficiency perspective through the use of radiographs and computed tomographic scans, correlating the anatomic findings with the results of pulmonary function tests. The secondary purpose was to describe the natural history of these patients with respect to limited chest and thoracic spine growth leading to thoracic insufficiency syndrome with restrictive pulmonary disease.

Materials and Methods

The research protocol was approved by our institutional review board. The study design was prospective, and patients were accepted from 1996 until 2003. Patients were recruited from the neonatal intensive care units and perinatology clinics throughout Puerto Rico. Inclusion criteria were an anteroposterior chest radiograph and a whole spine radiograph showing multiple congenital vertebral segmentation and formation defects associated with bilateral symmetric rib fusion (a fan-like configuration).

In addition, we retrospectively collected data from the genetic clinics in Puerto Rico to study the patients in whom the diagnosis of spondylothoracic dysplasia had already been made. The total study group consisted of eleven patients who were followed prospectively and nine patients who were followed retrospectively.

Data Collection (Table I)

Physical Examination

Evaluation of the patients consisted of a clinical history, including respiratory history of pneumonia episodes, hospitalizations, and the need for oxygen support. Physical examination included determination of the respiratory rate, lung auscultation, anthropomorphic measurements (height, weight, chest circumference at the nipple line, and limb length), the thumb excursion test to evaluate thoracic wall expansion during respiration¹, and the Adams forward bend test to assess for the presence of a posterior rib hump.

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TABLE I Data Collection Methods

Data Collection Methods and Specific Evaluations	Comments
Physical examination
Lung auscultation/respiratory rate
Anthropomorphic measures	Height, weight, chest circumference, limb length
Thumb excursion test	Evaluation of thoracic wall movement during respiration
Adams forward bend test	Evaluation of rib hump
Imaging
Standing anteroposterior and lateral radiographs of the spine and chest (n = 17)	Cobb angle, sagittal measurements, space available for lung ratio
Supine anteroposterior and lateral radiographs of the spine and chest (n = 3)	Cobb angle, sagittal measurements, space available for lung ratio
Cervical spine radiograph
Computed tomography	Vertebral body and spinal canal sagittal and coronal measures, sagittal depth of thorax, sternal length, liver and spleen longitudinal diameter, thoracic spinal height, lumbar spinal height, chest symmetry, anatomic lung-diaphragm configuration, volume of lung parenchyma
Pulmonary function
Forced vital capacity (n = 13)
Forced expiratory volume in one second (n = 13)

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TABLE I Data Collection Methods

Data Collection Methods and Specific Evaluations	Comments
Physical examination
Lung auscultation/respiratory rate
Anthropomorphic measures	Height, weight, chest circumference, limb length
Thumb excursion test	Evaluation of thoracic wall movement during respiration
Adams forward bend test	Evaluation of rib hump
Imaging
Standing anteroposterior and lateral radiographs of the spine and chest (n = 17)	Cobb angle, sagittal measurements, space available for lung ratio
Supine anteroposterior and lateral radiographs of the spine and chest (n = 3)	Cobb angle, sagittal measurements, space available for lung ratio
Cervical spine radiograph
Computed tomography	Vertebral body and spinal canal sagittal and coronal measures, sagittal depth of thorax, sternal length, liver and spleen longitudinal diameter, thoracic spinal height, lumbar spinal height, chest symmetry, anatomic lung-diaphragm configuration, volume of lung parenchyma
Pulmonary function
Forced vital capacity (n = 13)
Forced expiratory volume in one second (n = 13)

Imaging

Anteroposterior and lateral whole spine and chest radiographs were made to evaluate the cervical, thoracic, and lumbar spine and rib cage anatomy. Cervical radiographs were made, but the superimposition of the shoulders and the mandible combined with the extremely short neck made conventional radiographic evaluation inadequate. The Cobb angle²², sagittal measurements such as lordosis and kyphosis, and the space available for the lung ratio¹ were measured.

Computed tomographic scans of the chest, the abdomen, and the entire spine were made for all patients with use of an Xvision EX scanner (Toshiba, Tokyo, Japan); the scans consisted of 2-mm cuts that were made while the patient was breathing spontaneously. Computed tomographic data reduction with use of two-dimensional sagittal and coronal planes and three-dimensional reformations was performed with use of Vitrea workstation software 2.1 (Vital Images, Minnetonka, Minnesota). Data were validated with the standard nomenclature by designating the caudalmost vertebra with a costovertebral joint as being equivalent to the T12 level and the caudalmost lumbar vertebra as being equivalent to the L5 level.

The sagittal depth of the thorax was calculated by measuring the distance from the anterior surface of the T12-equivalent vertebral body to the posterior surface of the sternum. The sternal length and the longitudinal diameters of the liver and spleen were compared with normative standards. The thoracic spinal height was calculated by measuring the distance from the top of the first thoracic vertebra to the bottom of the T12-equivalent vertebra, and the lumbar spinal height was calculated by measuring the distance from the bottom of the T12-equivalent vertebra to the bottom of the most caudal lumbar vertebra²³. To evaluate chest symmetry, the posterior hemithoracic symmetry ratio¹ and thoracic and spinal rotation¹ were measured through the T12-equivalent vertebra.

The anatomic lung-diaphragm configuration was determined on the basis of the sagittal costophrenic depth ratio. Calculation of the sagittal costophrenic depth ratio involved measuring the distances from the apex of each lung to both the anterior and posterior costodiaphragmatic recesses in the sagittal plane at the midclavicular line. Subsequently, the ratio of the anterior distance to the posterior distance was calculated. The anterior costodiaphragmatic insertion is usually at the sternum xiphoid (the T9 level), and the posterior costodiaphragmatic insertion is from the T12 level to the L2 level. The normal value for this ratio is expected to be <1 (Figs. 1-A and 1-B).

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Fig. 1-A Fig. 1-B: Figs. 1-A and 1-B Sagittal computed tomographic scans of the chest at the midclavicular level. Lines a and b demonstrate the measurements of the distances from the apex of each lung to both the anterior (a) and posterior (b) costodiaphragmatic recesses. Fig. 1-A Normal sagittal costophrenic depth ratio. Fig. 1-B Abnormal sagittal costophrenic depth ratio seen in spondylothoracic dysplasia.

The volume of the lung parenchyma was determined with use of the technique described by Schlesinger et al.²⁴ (Fig. 2-A), and the findings were compared with the normative data reported by Gollogly et al.²⁵. In order to describe the abnormal positioning of the lungs into the abdomen in our patients, we determined the volume of the portion of each lung that was caudad to the transverse plane of the inferior posterior diaphragmatic insertion point at the midclavicular line (Fig. 2-B).

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Fig. 2-A Fig. 2-B: Fig. 2-A Computed tomographic scan reconstruction of the lung in a patient with spondylothoracic dysplasia, showing shortening of the posterior thoracic spine and anterior displacement of the lung below T12. Fig. 2-B Sagittal computed tomographic scan of the chest at the midclavicular level. The percentage of lung caudad to T12 is calculated as a/a+b.

Pulmonary Function

Spirometric (flow-volume) tests without bronchodilators were performed by a single respiratory care technician and were supervised by a pulmonary medicine physician (J.R.) in thirteen patients who were at least seven years old (average age, twenty-one years; range, seven to forty-nine years). Forced vital capacity (FVC) and forced expiratory volume in one second (FEV1) were measured with use of a Medgraphics Elite D-system 2000 model 83003-004 pulmonary function test machine with BreezeSuite software (Medical Graphics, St. Paul, Minnesota). Measurements were established according to the Knudson criteria²⁶. These data were analyzed with use of predicted values that were based on arm span as the height of the patients was shortened because of the congenital anomaly of the spine^27,28. The tests were repeated for seven adult patients at the time of the five-year follow-up.

Distributions of variables were given as means and ranges. Statistical comparisons were performed with use of the Student t test. Adjustments for one or two-tailed t tests as well as for paired or homoscedastic tests were performed in the appropriate situations. The level of significance was set at p < 0.05.

Results

Sample

We identified a total of twenty-eight patients who fulfilled Solomon's diagnostic criteria for spondylothoracic dysplasia²⁰. Nineteen of the twenty-eight patients were prospectively identified through the neonatal intensive care units early in the newborn period. Eight (42%) of the nineteen prospectively identified patients had died in the neonatal period as a result of respiratory complications before computed tomographic scans were made and therefore were not included in the study. Computed tomographic scans were made for the remaining eleven patients (average age, three years and nine months; range, four months to nine years), who constituted the prospective portion of the study. The study also included nine patients (average age, twenty-five years; range, twelve to forty-nine years) in whom the diagnosis of spondylothoracic dysplasia had been made retrospectively through the genetic clinics.

The study group included seven preschool-aged children (average age, 2.5 years; range, four months to four years), six school-aged children (average age, 10.2 years; range, seven to fourteen years), and seven adults (average age, 28.7 years; range, eighteen to forty-nine years).

History and Physical Examination

After the hospitalization following delivery, there was an average of 4.2 emergency room visits (range, one to ten visits) per patient during the first year of life because of respiratory problems. No patient required mechanical ventilation; however, nonmechanical respiratory support was necessary during 56% of the visits. The number of emergency room visits decreased to an average of two per year after the first year of life.

Vital signs were normal for age, with an appropriate respiratory rate at rest. The lungs were clear to auscultation. All patients had a protuberant abdomen with no evidence of visceromegaly (Figs. 3-A and 3-B). The lower costal margins of the rib cage extended abnormally downward close to the top of the iliac crests in all twenty patients.

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Fig. 3-A Fig. 3-B: Figs. 3-A and 3-B Lateral and posteroanterior clinical photographs of an eight-year-old girl with spondylothoracic dysplasia.

The average height was 115.7 cm (range, 44.5 to 155.96 cm), and the average height according to age was in the 1.15 percentile (range, first to third percentile). The average weight was 24.41 kg (range, 4 to 51 kg), and the average weight according to age was in the 1.1 percentile (range, first to third percentile)²⁹. To assess the possible effect of body weight on oxygen demand for these patients with restrictive lung disease, the body mass index was calculated (kg/m²). The average body mass index was 18.15 (range, 12 to 25). Following the guidelines of the United States National Heart, Lung, and Blood Institute³⁰, 70% of our patients were underweight for their height, with the remaining 30% having a normal weight for their height. Both upper and lower limb measurements were within normal parameters for age and gender when compared with growth references databases³¹.

Evaluation of the musculoskeletal system revealed that the cervical region was clinically rigid and extremely short. A low posterior hairline was observed in all patients. The average thoracic circumference at the nipple line was 65.2 cm (range, 34.5 to 103 cm), which was in the thirty-fourth percentile (range, first to ninety-ninth percentile). The ratio of chest circumference to height³² was an average of 0.634 (range, 0.486 to 0.779), compared with an expected value of 0.521 (range, 0.476 to 0.648) (p < 0.0001). There was no difference between children and adults (p = 0.856). The result on the thumb excursion test¹ was "0" bilaterally for all patients, indicating that respiration was totally diaphragmatic, with no contribution from secondary breathing due to a stiff rib cage. The Adams forward bend test showed mild unilateral thoracolumbar prominences in five patients. All patients had clinical thoracolumbar lordosis.

Imaging

Radiographs

Radiographs revealed that the rib cage was asymmetrically shortened, with the posterior aspect more severely affected than the anterior aspect. The fusion of all ribs at the costovertebral junction was evident (Figs. 4-A and 4-B), and there was an average of only six (range, five to eight) thoracic vertebrae. The vertebrae had multiple segmentation and formation defects such as block, wedge, and hemivertebrae as classified by Winter et al.³³. The thoracic region had a predominance of segmentation defects (block vertebrae), whereas the lumbar region had a predominance of formation defects (hemivertebrae). Lumbar spine radiographs revealed a variable number of lumbar vertebrae (average, five vertebrae; range, four to six vertebrae).

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Fig. 4-A Fig. 4-B: Fig. 4-A Anteroposterior radiograph of the chest and spine, showing all of the vertebral segmentation and formation defects with fusion of all ribs at the same costovertebral junction. Fig. 4-B Lateral radiograph of the spine, made with the patient standing, showing the anterior lung displacement.

Only five of the twenty patients had scoliosis, all in the thoracolumbar region. There were three left-sided curves and two right-sided curves, with an average Cobb angle of 25° (range, 15° to 35°). On the sagittal view, the patients showed a thoracolumbar lordosis measured from the higher thoracic vertebra to the top of sacrum, with an average curvature of 42° (range, 25° to 80°). The average space available for the lungs ratio¹ was 110.6% (range, 100% to 128%) for patients with scoliosis, compared with 100% for patients without scoliosis (p < 0.001). There was an average of ten ribs (range, seven to twelve ribs) per hemithorax.

Computed Tomography

Computed tomographic scans of the cervical spine revealed that the atlas fused to the occiput and the axis fused as a block to the remaining cervical vertebrae in all patients. The atlantoaxial articulation was normal. Thus, it was impossible to determine how many cervical vertebrae were actually present (Figs. 5-A and 5-B).

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Fig. 5-A Fig. 5-B: Fig. 5-A Lateral cervical radiograph of a patient with spondylothoracic dysplasia, showing fusion of the cervical vertebrae except at the C1-C2 joint. Fig. 5-B Lateral spinal computed tomographic scan reconstruction at the sternal level, showing the lack of segmentation mostly at the cervical level.

On computed tomographic scans, the T1-S1 spinal segment was an average of 13.14 cm (range, 8 to 20.4 cm) and was an average of only 14% of the standing height. The normal percentage ranges from 32.3% of the length of newborns to 25.5% of the standing height in adults³². The average thoracic spinal height was 5.07 cm (range, 3 to 8.9 cm) and was equivalent to an average of 24.2% (range, 19.2% to 33.3%) of the predicted normal value²³. Despite multiple vertebral anomalies, the lumbar spinal height on computed tomographic scans was an average of 8.7 cm (range, 5 to 11.5 cm) and was equivalent to an average of 70.1% (range, 45% to 116%) of the predicted normal value²³ (p < 0.0001).

The typical appearance of the thoracic vertebrae was that of a body with normal width but less than half of the normal sagittal depth and a normal spinal canal³⁴ (Fig. 6 and Table II). This configuration was observed in the children as well as in the adults, with no difference noted between age-groups, suggesting that the thoracic vertebral configuration is constant throughout all age-groups. The ribs were symmetrically fused at the costovertebral junction, giving the appearance of a common origin for all of the ribs at the shortened thoracic spine (Figs. 7-A, 7-B, and 7-C).

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Fig. 6: Transverse computed tomographic scan at the T12-equivalent vertebra, demonstrating normal vertebral body width but less than half of the normal sagittal depth and a normal spinal canal.

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Fig. 7-A Fig. 7-B Fig. 7-C: Anteroposterior (Fig. 7-A), lateral (Fig. 7-B), and posteroanterior (Fig. 7-C) computed tomographic scans of the entire spine with three-dimensional reformation. All ribs are symmetrically fused at the costovertebral junction, giving the appearance of a common origin for all of the ribs at the shortened thoracic spine.

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TABLE II Upper End Plate and Spinal Canal Depth and Width Values of Vertebrae

	Average (mm)	Range (mm)	Norm Reference (mm)
Thoracic
Upper end plate
Width	40.13	36 to 44.6	39
Depth	13.47	11.2 to 11.8	32.8
Width/depth ratio	2.98	2.53 to 3.81	1.2
Spinal canal
Width	23.2	20 to 26.2	22.2
Depth	12.4	15.8 to 21.0	18.1
Width/depth ratio	1.87		1.2
Lumbar
Upper end plate
Width	44.9	38.7 to 51	47.3
Depth	21.4	17.2 to 29	34.7
Width/depth ratio	2.10		1.36
Spinal canal
Width	31.1	28 to 36	27.1
Depth	19.9	16.2 to 33	19.7
Width/depth ratio	1.56		1.38

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TABLE II Upper End Plate and Spinal Canal Depth and Width Values of Vertebrae

	Average (mm)	Range (mm)	Norm Reference (mm)
Thoracic
Upper end plate
Width	40.13	36 to 44.6	39
Depth	13.47	11.2 to 11.8	32.8
Width/depth ratio	2.98	2.53 to 3.81	1.2
Spinal canal
Width	23.2	20 to 26.2	22.2
Depth	12.4	15.8 to 21.0	18.1
Width/depth ratio	1.87		1.2
Lumbar
Upper end plate
Width	44.9	38.7 to 51	47.3
Depth	21.4	17.2 to 29	34.7
Width/depth ratio	2.10		1.36
Spinal canal
Width	31.1	28 to 36	27.1
Depth	19.9	16.2 to 33	19.7
Width/depth ratio	1.56		1.38

The typical appearance of the lumbar vertebrae was that of a body with normal width but decreased depth and a spinal canal of normal depth with a slightly increased width³⁵. This configuration was observed in the children as well as in the adults, suggesting that the lumbar vertebral configuration is also stable throughout growth. The lumbar vertebrae had anterior and posterior sagittal clefts identical to the cervical and thoracic vertebrae (Fig. 8 and Table II). The sacrococcygeal region was spared from any abnormality. Computed tomographic analysis revealed no increase in hepatic or splenic dimensions.

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Fig. 8: Transverse computed tomographic scan at the L5-equivalent vertebra, demonstrating a body with normal vertebral width but decreased depth and a spinal canal of normal depth with a slightly increased width.

Axial thoracic computed tomographic scans demonstrated variability in the thoracic cage configuration: eleven were triangular, seven were rectangular, one was round, and one was unclassifiable. The anteroposterior diameter of the chest as measured at the level of the T12-equivalent vertebra (the sternovertebral distance) was decreased (average, 6.79 cm; range, 0.5 to 9.2 cm), with the average value being below the 2.5th percentile for age (p < 0.0001)³². The mean posterior hemithoracic symmetry ratio was 1.17 (range, 1 to 1.5), with 1.0 being normal¹. The mean amount of thoracic rotation was 9.9° (range, 0° to 17.9°), and the mean spinal rotation was 8.8° (range, 0° to 16.3°), with 0° being the normal value for both measurements¹. The sternal length from the top of the manubrium to the bottom of the body was measured in the midsagittal plane. The ratio of sternal length to patient height (arm span) was an average of 8.67% (range, 4.9% to 14.3%), and this was not different from the value of 9.56% expected in the general population (p = 0.12)³⁶.

In normal diaphragmatic anatomy, the posterior diaphragmatic insertion is caudad to the anterior insertion because of the fact that the posterior thoracic wall is much longer than the anterior wall³⁷. In our patients, this was reversed, with the anterior costodiaphragmatic insertion being caudad to the posterior insertion. The average sagittal costophrenic depth ratio was 1.75 (range, 0.88 to 2.73) for the right hemithorax and 1.65 (range, 1 to 2.64) for the left hemithorax, compared with the expected ratio of <1.

The costovertebral joints appeared to be replaced by a complete fusion of the head, neck, and tubercle of the ribs with the costal facet, pedicle, and transverse process of the thoracic vertebra (Fig. 9).

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Fig. 9: The costovertebral joints were replaced by a complete fusion of the head, neck, and tubercle of the ribs with the costal facet, pedicle, and transverse process of the thoracic vertebra.

The trachea had a normal configuration in eleven patients and was shifted to the right by an average of 12.4 mm (range, 4.8 to 26.6 mm) from the midline in the remaining nine patients. There was no evidence of lung bronchiectasis or atelectasis.

Lung volume measurements on computed tomographic scans revealed extremely small lungs when compared with the expected volumes for age and gender, with all values below the third percentile of normal²⁵ and with an average total lung volume of 242.48 cm³ (range, 91.98 cm³ to 473.2 cm³). The lung volumes were an average of 28% (range, 15.4% to 41%) of the expected values for age and gender. The anterior descent of the right lung inferior to the transverse plane of the posterior diaphragmatic insertion point accounted for a mean of 35.9% (range, 13.1% to 62.7%) of the right lung volume, and the anterior descent of the left lung accounted for a mean of 30.2% (range, 9.9% to 47.9%) of the left lung volume (Fig. 2-B).

Spirometric (flow-volume) tests were performed for six children who were more than seven years of age and for seven adults. The spirometric reference values are described as a function of the patient's height, age, and gender^28,38. For patients with scoliosis, the normalized height can be approximated by utilizing arm span measurements to derive normal pulmonary function values^1,27,28. Use of the arm span correction for normalized height revealed that the average spirometric values were 27.9% (range, 17% to 48%) of the predicted forced vital capacity (FVC), 29.5% (range, 17% to 51%) of the predicted forced expiratory volume in the first second (FEV1), and 0.92 (range, 0.81 to 1.0) for the FEV1/FVC ratio, demonstrating a severe restrictive respiratory pattern. Seven patients with an average age of 28.7 years (range, eighteen to forty-nine years) had pulmonary function tests at minimum of five years of follow-up, and neither the FVC nor FEV1 changed significantly (p = 0.56), suggesting that the restrictive lung disease is stable in adults.

Discussion

Spondylothoracic dysplasia is a syndrome in which bilateral chest wall deformity due to costovertebral rib fusions with shortening of the thoracic spine results in thoracic insufficiency syndrome. All of our patients had abnormal respiratory function because of the presence of a stiff, fused chest wall that could not contribute to secondary breathing, severely reduced thoracic volume, and restricted lung growth. Most patients with spondylothoracic dysplasia described in the previous medical literature had a poor prognosis, with a nearly 100% mortality rate and a mean age of 1.5 years at the time of death from respiratory causes^{3,4,14,18,20,39-44}. In contrast, Cornier et al.⁴⁵, in a 2004 report on a series of twenty-seven patients with spondylothoracic dysplasia, noted an improvement in the survival rate, with a mortality rate resulting from respiratory disease of 44% and with all deaths occurring during the first year of life. The reasons for the decrease in the mortality rate are unclear but may be due to modern neonatal and pediatric intensive care capabilities. It is surprising how well our older patients have done clinically with severe restrictive lung disease secondary to a decreased thoracic height (24% of expected), diminished lung volume (28% of expected), and a low vital capacity (averaging only 27.9% of expected). Pehrsson et al.⁴⁶ suggested that a vital capacity of <45% and severe scoliosis were risk factors for respiratory failure in late adulthood, so it would be expected that a substantial proportion of our adult patients would have serious respiratory manifestations⁴⁷; however, at the time of the latest follow-up, they were clinically stable with an adequate quality of life and did not require supplemental oxygen.

We believe that the low to normal body mass index helps these patients to tolerate their restrictive lung disease due to thoracic insufficiency syndrome. Hayek et al., in 1999, reported on a long-term survivor of spondylothoracic dysplasia, a thirty-three-year-old obese woman of Puerto Rican descent who was living in the northeastern United States with a poor quality of life and who required constant supplemental oxygen therapy⁸. It is well known that obesity increases mortality rates⁴⁸ and can severely affect pulmonary function and reduce exercise capacity as a result of its harmful effects on lung volumes and pulmonary mechanics. In the present series, all patients were either slender or of normal weight (with a body mass index of 12 to 25). An ideal or even low body weight for height poses less aerobic demand on the respiratory system, perhaps allowing good clinical function in these patients. Additional clinical studies in which the pulmonary function and clinical health of patients with spondylothoracic dysplasia and an ideal body weight are compared with those in patients with a higher-than-ideal body weight would be useful.

It is also possible that the unique thoracic anatomy associated with spondylothoracic dysplasia syndrome may also help to explain these patients' unexpected survival and adequate quality of life. The volume depletion deformity⁴⁹ of the thorax was symmetrical shortening; however, the abnormal orientation of the diaphragm and the broad-based abnormal shape of the lung may have helped to protect the patients from the effects of the restrictive lung disease. Normally, the posterior thoracic wall is longer than the anterior wall³⁷, resulting in a posteroinferior thoracic base formed by the diaphragm that slopes upward anterosuperiorly. The thoracic spine, which is the central structure of the posterior chest wall and defines thoracic height, should measure 12 cm in normal newborns and should grow to approximately 28 cm in adults³². In our series, the height of the thoracic spine ranged from 3 cm in the newborn to only 8.9 cm in adulthood. Remarkably, the longest thoracic spine in our series was still 3.1 cm shorter than the thoracic spine of a normal newborn. The average thoracic spine height was only 24% of normal for our patients, indicating a severe posterior restriction of thoracic volume. Normally, the T1-S1 spinal segment ranges from 32.3% of the length of newborns to 25.5% of the standing height in adults³², but in our patients this spinal segment represented an average of only 14% of the standing height. Interestingly, the spinal shortening in our patients appeared to occur in a cephalocaudal pattern, with the thoracic region more severely affected than the lumbar region with regard to the number of vertebrae as well as the relative spinal heights of the thoracic and lumbar spine. The sternum, which forms the anterior border of the thorax, was of normal length in our patients. The thorax was narrow in the sagittal plane (2.5th percentile) secondary to the rib cage deformity and the spinal lordosis pushing into the chest. The shortened spine posteriorly reversed the normal slope of the inferior thoracic base, sloping downward anteroinferiorly. Consequently, the diaphragm had a more inferior insertion in the anterior aspect of the thorax, resulting in a relatively longer anterior thorax.

In an attempt to further elucidate the importance of this finding, we compared the relative heights of both anterior and posterior hemithoraces and established a ratio of the anterior height to the posterior height. According to what is expected from the normal chest anatomy, the sagittal costrophrenic depth ratio should be <1. The analysis of our population demonstrated an average sagittal costrophrenic ratio of 1.8. The thorax was slanted obliquely downward and anteriorly, with approximately one-third of the lung volume caudad to the level of the T12-equivalent vertebra. In summary, the patients had a short posterior thorax height with a large anterior slanted base area.

Although the thoracic height (24% of expected) and the total lung volume (28% of expected) remain small in these patients, the unique configuration of the thorax may be advantageous for clinical ventilation. The change of the thoracic volume is mediated by the diaphragm (primary breathing) and by intercostal muscle contraction (secondary breathing). Deficiencies in either affect respiration and contribute to thoracic insufficiency syndrome. Secondary breathing and its contribution to the vital capacity were completely absent in these patients, as there was complete fusion of the ribs. Primary breathing mediated by the diaphragm was the only respiratory mechanism available to these patients. The diaphragm is highly dependent on its precontraction length and anatomic arrangement and the balance of energy supply and demand⁵⁰. Lung expansion is more efficient during breathing when there is a larger-than-normal surface area of lung in close apposition to the diaphragm^50,51. In addition, the lung base is the best-perfused area of the lungs and the most efficient in blood oxygenation⁵². Consequently, an abnormally broad lung expanded by a diaphragm with a larger-than-normal surface area may increase blood oxygenation beyond what would be expected for a limited amount of air exchange^50-52. We could not measure diaphragmatic mechanics or diaphragm surface area. The actual determinants of the ideal shape, volume, and optimal biomechanics of the thorax await further investigation.

Previous investigators have characterized the spine in patients with spondylothoracic dysplasia with use of radiographs only and have described segmentation and formation defects of the spine with bilateral fusion of all of the ribs at the costovertebral junction, giving the thorax a fan-like (or crab) appearance^3,4,20,39-44. Our group is the first, to our knowledge, to study the three-dimensional anatomy of the spine in patients with spondylothoracic dysplasia with use of computed tomographic scan analysis. The cervical spine in these patients is very difficult to visualize on plain radiographs, but three-dimensional reconstructions with use of computed tomographic scans demonstrated fusion of C1 to the skull and fusion from C2 caudally, leaving C1-C2 as the sole cervical spine joint. With an increased life span of these patients, this C1-C2 joint may have development of degenerative arthritis or instability, and, if symptomatic, it should best be studied with computed tomographic scan analysis. The thoracic spine was also severely affected, with the primary malformation being block vertebrae associated with an abnormal number of vertebrae (ranging from eight to only five), representing an average of only 24.2% of normal thoracic spinal height. While the vertebrae were relatively normal in width, they were relatively thin in the sagittal plane, with a depth of only 41% of normal. This should be appreciated if spinal instrumentation involving thoracic pedicle screws is being considered for these patients. Surprisingly, the thoracic spinal canal was normal in width and depth for age, in contrast to some other forms of dwarfism and skeletal dysplasia. The lumbar spine was somewhat less affected, with the number of vertebrae being close to normal, varying between four and six, but there was an average of four lumbar hemivertebrae per patient. Like the thoracic vertebrae, the lumbar vertebrae were of relatively normal width but were narrow in sagittal depth. The lumbar spinal canal was of normal depth and was slightly wider than normal. The relative dimensions of the vertebrae and the spinal canal were similar for both children and adults, suggesting that they do not change with growth. Previous reports on spondylothoracic dysplasia with spinal deformity⁷ have suggested that these patients are predisposed to neurological symptoms because of the presence of thoracic kyphosis and spinal canal stenosis. This is completely contrary to our findings of thoracolumbar lordosis with a normal spinal canal and no neurological signs or symptoms.

Coronal plane spinal deformity in the present series was minimal. Only 25% of our patients had scoliosis. All curves were thoracolumbar, averaging 25°, and none required treatment. While asymmetric tethering from unilateral fused ribs in spondylocostal dysostosis does contribute to curve progression^1,2,53, symmetrical tethering resulting from bilateral fused ribs in spondylothoracic dysplasia extending into the thoracic block vertebrae may help to stabilize the thoracic spine and, although the lumbar spine often had many hemivertebrae, they were almost all incarcerated and were unlikely to cause substantial progression. Scoliosis appears to be a minor problem in spondylothoracic dysplasia.

To our knowledge, the natural history of thoracic insufficiency due to spondylothoracic dysplasia in patients with extensive follow-up has not been previously described. To our knowledge, our study represents the largest series of living patients with spondylothoracic dysplasia to have been reported. Although these patients were doing well clinically, they had severe restrictive lung disease due to thoracic insufficiency syndrome. None of the patients required supplemental oxygen or respiratory support. Medical evaluations due to respiratory problems decreased substantially after the first year of life. It remains unclear as to why some patients with spondylothoracic dysplasia die early and others survive into adult life.

Due to the severe shortening of the thorax secondary to congenital loss of height of the thoracic spine, patients with spondylothoracic dysplasia may help to provide a natural history model of thoracic insufficiency syndrome that can be seen following early spine fusion for the treatment of childhood spinal deformity. A common denominator between children with an early surgical spinal fusion and patients with spondylothoracic dysplasia is the decrease in the height of the thorax. One important unanswered question is how much the height of the thoracic spine at skeletal maturity contributes to lung volume and vital capacity. If this relationship were better understood, growth tables³² could predict the final thoracic spinal height at skeletal maturity. Thus, the effect of spinal height at skeletal maturity on lung volume and vital capacity could be estimated. Our data (not shown) do suggest that the loss of thoracic spinal height correlates with loss of both computed tomographic scan lung volume and vital capacity, so this is an important factor to consider when a spinal fusion is planned for a young child. The precise relationship between all of these complex variables awaits an animal model of thoracic insufficiency syndrome.

Several recent reports have described poor pulmonary outcome when a child undergoes early spinal fusion^54-56. The natural history of the thoracic insufficiency syndrome in our patients with spondylothoracic dysplasia may be helpful for understanding the poor growth and function of the thorax associated with an adverse pulmonary outcome in children who have fusion of the thoracic spine early in life.

The present study had two weaknesses. The first was the size of the sample. As is the case with any autosomal recessive genetic disorder^3,4,45, it is difficult to obtain a large affected population that will allow more data to be acquired. The second was the lack of more imaging studies during the neonatal period, particularly for children who did not survive this period.

In conclusion, spondylothoracic dysplasia has a unique pathoanatomy, resulting in severe restrictive¹ lung disease. Mortality is high, but patients who survive past infancy have the potential for a good quality of life, despite continuing severe restrictive lung disease, and show no major progression of the congenital anomalies, including those in the spine. This disease may serve as a model to determine the natural history of thoracic insufficiency syndrome in patients with inhibitory effects of the growth of the spine due to either a congenital cause or secondary to surgical fusion early in life. Image Not Available

Acknowledgements

Note: The authors acknowledge the assistance of John Flynn, MD, M.J. Mulcahey, Randal Betz, MD, Josean Herrera-Soto, MD, and Abilio Reiss, MD, with the preparation of the study.

References

Campbell RM Jr, Smith MD, Mayes TC, Mangos JA, Willey-Courand DB, Kose N, Pinero RF, Alder ME, Duong HL, Surber JL. The characteristics of thoracic insufficiency syndrome associated with fused ribs and congenital scoliosis. J Bone Joint Surg Am.2003;85:399-408.85399 2003 [PubMed][CrossRef]

Campbell RM Jr, Smith MD, Mayes TC, Mangos JA, Willey-Courand DB, Kose N, Pinero RF, Alder ME, Duong HL, Surber JL. The effect of opening wedge thoracostomy on thoracic insufficiency syndrome associated with fused ribs and congenital scoliosis. J. Bone Joint Surg Am.2004;86:1659-74.861659 2004

Lavy NW, Palmer CG, Merritt AD. A syndrome of bizarre vertebral anomalies. J Pediatr.1966;69:1121-5.691121 1966 [CrossRef]

Moseley JE, Bonforte RJ. Spondylothoracic dysplasia—a syndrome of congenital anomalies. Am J Roentgenol Radium Ther Nucl Med.1969;106:166-9.106166 1969

Pérez-Comas A, García-Castro JM. Occipito-facial-cervicothoracic-abdomino-digital dysplasia; Jarcho-Levin syndrome of vertebral anomalies. Report of six cases and review of the literature. J Pediatr.1974;85:388-91.85388 1974 [CrossRef]

Jarcho S, Levin PM. Hereditary malformations of the vertebral bodies. Bull Johns Hopkins Hosp.1938;62:216-26.62216 1938

Mooney JF 3rd, Emans JB. Progressive kyphosis and neurologic compromise complicating spondylothoracic dysplasia in infancy (Jarcho-Levin syndrome). Spine.1995;20:1938-42.201938 1995 [CrossRef]

Hayek S, Burke SW, Boachie-Adjei O, Bisson LJ. Jarcho-Levin syndrome: report on a long-term follow-up of an untreated patient. J Pediatr Orthop B.1999;8:150-3.8150 1999 [CrossRef]

Hatakeyama K, Fuse S, Tomita H, Chiba S. Jarcho-Levin syndrome associated with a complex congenital heart anomaly. Pediatr Cardiol.2003;24:86-8.2486 2003

Schulman M, Gonzalez MT, Bye MR. Airway abnormalities in Jarcho-Levin syndrome: a report of two cases. J Med Genet.1993;30:875-6.30875 1993 [CrossRef]

Poor MA, Alberti O Jr, Griscom NT, Driscoll SG, Holmes LB. Nonskeletal malformations in one of three siblings with Jarcho-Levin syndrome of vertebral anomalies. J Pediatr.1983;103:270-2.103270 1983 [CrossRef]

Rastogi D, Rosenzweig EB, Koumbourlis A. Pulmonary hypertension in Jarcho-Levin syndrome. Am J Med Genet.2002;107:250-252.107250 2002 [CrossRef]

Karnes PS, Day D, Berry SA, Pierpont ME. Jarcho-Levin syndrome: four new cases and classification of subtypes. Am J Med Genet.1991;40:264-70.40264 1991 [CrossRef]

Heilbronner DM, Renshaw TS. Spondylothoracic dysplasia. A case report. J Bone Joint Surg Am.1984;66:302-3.66302 1984

Apuzzio JJ, Diamond N, Ganesh V, Desposito F. Difficulties in the prenatal diagnosis of Jarcho-Levin syndrome. Am J Obstet Gynecol.1987;156:916-8.156916 1987

Tolmie JL, Whittle MJ, McNay MB, Gibson AA, Connor JM. Second trimester prenatal diagnosis of the Jarcho-Levin syndrome. Prenat Diagn.1987;7:129-34.7129 1987 [CrossRef]

Bannykh SI, Emery SC, Gerber JK, Jones KL, Bernirschke K, Masliah E. Aberrant Pax1 and Pax9 expression in Jarcho-Levin syndrome: report of two Caucasian siblings and literature review. Am J Med Genet A.2003;120:241-6.120241 2003

Mortier GR, Lachman RS, Bocian M, Rimoin DL. Multiple vertebral segmentation defects: analysis of 26 new patients and review of the literature. Am J Med Genet.1996;61:310-9.61310 1996 [CrossRef]

Martínez-Frías ML, Urioste M. Segmentation anomalies of the vertebras and ribs: a developmental field defect: epidemiologic evidence. Am J Med Genet.1994;49:36-44.4936 1994 [CrossRef]

Solomon L, Jiménez RB, Reiner L. Spondylothoracic dysostosis: report of two cases and review of the literature. Arch Pathol Lab Med.1978;102:201-5.102201 1978

Franceschini P, Grassi E, Fabris C, Bogetti G, Randaccio M. The autosomal recessive form of spondylocostal dysostosis. Radiology.1974;112:673-5.112673 1974

Cobb JR. Outline for the study of scoliosis. Instr Course Lect.1948;5:261-75.5261 1948

Dimeglio A. Growth of the spine before age 5 years. J Pediatr Orthop B.1993;1:102-7.1102 1993

Schlesinger AE, White DK, Mallory GB, Hildeboldt CF, Huddleston CB. Estimation of total lung capacity from chest radiography and chest CT in children: comparison with body plethysmography. AJR Am J Roentgenol.1995;165:151-4.165151 1995

Gollogly S, Smith JT, White SK, Firth S, White K. The volume of lung parenchyma as a function of age: a review of 1050 normal CT scans of the chest with three-dimensional volumetric reconstruction of the pulmonary system. Spine.2004;29:2061-6.292061 2004 [CrossRef]

Knudson RJ, Lebowitz MD, Holberg CJ, Burrows B. Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis.1983;127:725-34.127725 1983

Johnson BE, Westgate HD. Methods of predicting vital capacity in patients with thoracic scoliosis. J Bone Joint Surg Am.1970;52:1433-9.521433 1970

Parker JM, Dillard TA, Phillips YY. Arm span-height relationships in patients referred for spirometry. Am J Respir Crit Care Med.1996;154:533-6.154533 1996

Saul RA, Seaver LH, Sweet KM, Geer JS, Phelan MC, Mills CM. Growth references: third trimester to adulthood. 2nd ed. Greenwood, SC: Greenwood Genetic Center; 1998. p 6-9. 1998

National Heart, Lung, and Blood Institute. Clinical practice guidelines. . Accessed 2005 March 12. 2005
http://www.nhlbi.nih.gov/guidelines

Saul RA, Seaver LH, Sweet KM, Geer JS, Phelan MC, Mills CM. Growth references: third trimester to adulthood. 2nd ed. Greenwood, SC: Greenwood Genetic Center; 1998. p 41-50. 1998

Dimeglio A, Bonnel F. Le rachis en croissance. Paris: Springer; 1990. 1990

Winter RB, Moe JH, Eilers VE. Congenital scoliosis. A study of 234 patients treated and untreated. J Bone Joint Surg Am.1968;50:1-47.501 1968

Panjabi MM, Takata K, Goel V, Federico D, Oxland T, Duranceau J, Krag M. Thoracic human vertebrae. Quantitative three-dimensional anatomy. Spine.1991;16:888-901.16888 1991 [CrossRef]

Panjabi MM, Goel V, Oxland T, Takata K, Duranceau J, Krag M, Price M. Human lumbar vertebrae. Quantitative three-dimensional anatomy. Spine.1992;17:299-306.17299 1992 [CrossRef]

Dwight T. Sternum as an index of sex, height, and age. J Anat Physiol.1890;24:527-35.24527 1890

Moore KL, Dalley AF 2nd, editors. Clinically oriented anatomy. 4th ed. Philadelphia: Lippincott Williams and Wilkins; 1999. p 60-115, 289-295. 1999

Pehrsson K, Danielsson A, Nachemson A. Pulmonary function in adolescent idiopathic scoliosis: a 25 year follow up after surgery or start of brace treatment. Thorax.2001;56:388-93.56388 2001 [CrossRef]

Pochaczevsky R, Ratner H, Perles D, Kassner G, Naysan P. Spondylothoracic dysplasia. Radiology.1971;98:53-8.9853 1971

McCall CP, Hudgins L, Cloutier M, Greenstein RM, Cassidy SB. Jarcho-Levin syndrome: unusual survival in a classical case. Am J Med Genet.1994;49:328-32.49328 1994 [CrossRef]

Herold HZ, Edlitz M, Baruchin A. Spondylothoracic dysplasia. A report of ten cases with follow-up. Spine.1988;13:478-81.13478 1988 [CrossRef]

Roberts AP, Conner AN, Tolmie JL, Connor JM. Spondylothoracic and spondylocostal dysostosis. Hereditary forms of spinal deformity. J Bone Joint Surg Br.1988;70:123-6.70123 1988

Trindade CE, de Nóbrega FJ. Spondylothoracic dysplasia in two siblings. A short neck and trunk due to vertebral body abnormalities along with abnormal ribs should suggest this rare syndrome. Clin Pediatr (Phila).1977;16:1097-9.161097 1977 [CrossRef]

Swietlinski J, Swist-Szulik K, Maruniak-Chudek I, Pyrkosz A. Spondylothoracic dysostosis associated with diaphragmatic hernia and camptodactyly. Genet Couns.2002;13:309-17.13309 2002

Cornier AS, Ramírez N, Arroyo S, Acevedo J, García L, Carlo S, Korf B. Phenotype characterization and natural history of spondylothoracic dysplasia syndrome: a series of 27 new cases. Am J Med Genet A.2004;128:120-6.128120 2004

Pehrsson K, Bake B, Larsson S, Nachemson A. Lung function in adult idiopathic scoliosis: a 20 year follow up. Thorax.1991;46:474-8.46474 1991 [CrossRef]

Pehrsson K, Larsson S, Oden A, Nachemson A. Long-term follow-up of patients with untreated scoliosis. A study of mortality, causes of death, and symptoms. Spine.1992;17:1091-6.171091 1992 [CrossRef]

Troiano RP, Frongillo EA Jr, Sobal J, Levitsky DA. The relationship between body weight and mortality: a quantitative analysis of combined information from existing studies. Int J Obes Relat Metab Disord.1996;20:63-75.2063 1996

Campbell RM Jr, Smith MD. Thoracic insufficiency syndrome and exotic scoliosis. J Bone Joint Surg Am.2007;89 Suppl 1:108-22.89 Suppl 1108 2007

Celli BR. Clinical and physiologic evaluation of respiratory muscle function. Clin Chest Med.1989;10:199-214.10199 1989

Loring SH, Mead J. Action of the diaphragm on the rib cage inferred from a force-balance analysis. J Appl Physiol.1982;53:756-60.53756 1982 [CrossRef]

Mettler FA Jr, Guiberteau MJ. Respiratory system. In: Mettler FA Jr, Guiberteau MJ, editors. Essentials of nuclear medicine imaging. 4th ed. Philadelphia: Saunders; 1998. p 191-2. 1998

Shahcheraghi GH, Hobbi MH. Patterns and progression in congenital scoliosis. J Pediatr Orthop.1999;19:766-75.19766 1999 [CrossRef]

Emans JB, Kassab F, Caubet JF, Hedequist D, Wohl ME, Campbell RM. Earlier and more extensive thoracic fusion is associated with diminished pulmonary function. Outcomes after spinal fusion of 4 or more thoracic spinal segments before age 5. Presented as a poster exhibit at the International Meeting of Advanced Spinal Techniques; 2004 Jul 1; Bermuda. 2004

Goldberg CJ, Gillic I, Connaughton O, Moore DP, Fogarty EE, Canny GJ, Dowling FE. Respiratory function and cosmesis at maturity in infantile-onset scoliosis. Spine.2003;28:2397-406.282397 2003 [CrossRef]

Karol L, Johnston C, Mladenov K, Schochet P, Walter SP. The effect of early thoracic fusion on pulmonary function on non-neuromuscular scoliosis. Read at the Annual Meeting of the Scoliosis Research Society; 2005 Oct 30; Miami, FL. 2005

Topics

lung ; forced vital capacity ; ribs ; scoliosis ; spine ; chest ; vertebrae ; thoracic spine ; restrictive lung disease ; jarcho-levin syndrome

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Norman Ramírez, Alberto S. Cornier, Robert M. CampbellJr., Simón Carlo, Sandra Arroyo, Jesse Romeu; Natural History of Thoracic Insufficiency Syndrome: A Spondylothoracic Dysplasia Perspective. The Journal of Bone & Joint Surgery. 2007 Dec;89(12):2663-2675.

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