Congenital scoliosis, or kyphoscoliosis, is an uncommon deformity in which developmental vertebral anomalies cause segmental abnormal lateral convex angulation of the spine. These vertebral anomalies, which appear at birth, result in localized impairment of anterior longitudinal spinal growth in the sagittal plane and increasing deformity as the child grows to skeletal maturity.1,2 In some patients, an asymmetrical impairment of anterior spinal growth result in kyphoscoliosis; however, most of the patients in the present study had scoliosis.
Clinicians and pathologists in the early 19th century observed that anatomical enlargement of the heart was often associated with spinal deformity.3,4 This observation was confirmed through several series of necropsies during the last century. Latham5 suggested that secondary displacement of the heart due to thoracic spine curvature may lead to the development of cardiac murmurs and extra cardiac sounds.
Electrocardiography was first systematically included into scoliosis diagnostics by Adorno and White.6 They observed right axis deviation in 17% of young patients with asymptomatic scoliosis. Towers and Zorab,7 in a study of 168 young patients with scoliosis, found common right and left axis deviation relative to normal readings as well as V2-V4 high-voltage QRS complexes. Results suggest that cardiac function and structure may be affected by scoliosis, especially congenital scoliosis. However, few studies of the effect of congenital scoliosis on cardiac function and structure have been published. Furthermore, correlative studies regarding apex vertebral rotation (AVR), side of curvature, or curvature severity in the coronal and sagittal planes have not been conducted in a large patient population.
The purpose of the present study was to assess the possible effects of AVR, side of convexity, severity of curvature in the coronal and sagittal planes, types of deformity, and sex on cardiac structure and function in adolescents with congenital scoliosis.
The medical records of 215 adolescent patients with congenital thoracic spine scoliosis followed and/or operated on at Peking Union Medical College Hospital from January 2003 to July 2007 were identified from a single institutional database. The patient study group consisted of 87 male and 128 female patients aged 10-19 years (age: 13.58=1=2.43 years). Within the 215 patients, deformities included 61 segmentation failures, 86 formation failures, and 68 mixed-type failures. All diagnoses were confirmed through complete sets of spine X-ray films, three-dimensional spine reconstructions, and surgeries.
The indications for surgical treatment included a poor prognosis if left untreated and severity of spinal deformity upon initial consult.8 Patients with scoliosis associated with congenital heart disease, myelo-meningocele, Marian's syndrome, neurofibromatosis, skeletal dysplasia, infection, trauma, or other secondary causes of scoliosis were excluded from the study.
M-mode and two-dimensional echocardiography and Doppler ultrasound of all patients were performed by the same sonographer with a GE Vivid7 scanner (GE Medical Systems, Horten, Norway) equipped with a 3.4-MHz phased array transducer. Recordings and measurements were made following international guidelines.9,10 The parameters evaluated included the followings: interventricular septum thickness at end-diastole (IVSd), posterior wall of left ventricle at end-diastole (LVPWd), left ventricular inner diameter at end-diastole (LVIDd), left ventricular inner diameter at end-systole (LVIDs), left atrial diameter (LAD), right ventricular diameter (RVD), diameter of aortic root (DAR), diameter of the arteria pulmonalis (DAP), ejection fraction (EF), and fractional shortening (FS).
Preoperative anteroposterior and lateral standing spine radiographs were obtained in conformed unification at our institution. Radiographic measurements were manually obtained by two surgeons using a double-blind method, and the mean value was used. Specifically, scoliosis and kyphosis were measured by using the Cobb method,11 and the degree of AVR (from I to IV) was measured by using the Nash-Moe method.
Patients with no cardiac or pulmonary disease were assigned to subgroups according to the following parameters: (1) AVR: Patients were classified into two subgroups (AVR ≤I° and AVR ≥I°). (2) Side of curvature: Patients with simple thoracic or double thoraco-lumbar curves were further assigned to two subgroups according to the side of the thoracic curvature. (3) Coronal plane Cobb angle: Patients were assigned to three subgroups according to curvature angle measured by the Cobb method in the coronal plane (<40°, group 1; 40°-80°, group 2; >80°, group 3). (4) Sagittal plane Cobb angle: Patients were classified into three subgroups according to kyphosis (<20°, group 1; 20°-40°, group 2; >40°, group 3). (5) Types of deformity: Patients were assigned to three subgroups according to type of deformity (group 1, segmentation failure; group 2, formation failure; group 3, mixed-type failure). (6) Sex: Patients with simple thoracic or double thoraco-lumbar curves were further assigned to two subgroups according to sex.
Standard statistical analyses were conducted. All data are expressed as mean±standard deviation. Independent-samples t test or one-factor analysis of variance was used, as appropriate, to determine differences between subgroups. Data were analyzed by using SPSS software for Windows (version 14.0; SPSS Inc., Chicago, IL, USA). P values <0.05 were considered statistically significant.
Adolescents with congenital scoliosis were assigned to two subgroups: those with an AVR <I° (group 1; n =74) and those with an AVR >I° (group 2; n=141). RVD was (16.89±3.39)mm in group 1 and (16.99±4.07)mm in group 2 (P=0.217); LAD was (27.30±4.09)mm in group 1 and (27.38±4.15)mm in group 2 (P=0.917); LVIDd was (41.00±4.89)mm in group 1 and (39.96±4.89)mm in group 2 (P =0.145), and LVIDs was (25.64±3.63)mm in group 1 and (25.07±3.18)mm in group 2 (P =0.231).
Parameters reflecting cardiac function were also comparable in both groups. EF ((67.58±4.95)% vs (68.08±5.45)%) and FS ((37.24±3.97)% vs (37.83±4.17)%) were shorter in group 2 than in group 1; however, the difference between groups was not significant. All variables were within the normal ranges of previous data for a healthy population without heart disease or scoliosis specific to the Chinese population.13
Side of curvature
Patients with simple thoracic or double thoraco-lumbar curves were further divided into two subgroups according to the side of the thoracic curvature: 129 patients had right-sided thoracic curvature, and 86 patients had left-sided thoracic curvature. The analysis of variance showed that the mean LVIDd ((41.47±4.90)mm vs (39.39±4.66)mm; P<0.001); LVIDs ((25.92±3.07)mm vs (24.80±3.45)mm; P=0.016), IVSd ((5.98±1.03)mm vs (5.66±0.98)mm; P=0.023), and LVPWd ((6.06±1.20)mm vs (5.61±0.98)mm; P=0.003) values were significantly greater in the left-sided group than in the right-sided group. RVD, LAD, DAR, and DAP—parameters reflecting cardiac function—were not significantly different between groups.
Coronal plane Cobb angle
Patients were divided into three subgroups according to the scoliotic Cobb angle: <40° (n=39), 40°-80° (n=120), and >80° (n=56). No significant differences were observed between groups 1 and 2. Groups 1 and 2 had similar cardiac structure and function parameters: RVD ((16.85±3.27)mm vs (17.14±4.03)mm; P=0.68), LAD ((26.44±4.36)mm vs (27.82±4.03)mm; P=0.07), LVIDs ((25.64±3.31)mm vs (25.53±3.39)mm; P=0.86), LVIDd ((40.31±4.61)mm vs (40.97±5.06)mm; P =0.46), IVSd ((5.95±1.07)mm vs (5.73±0.99)mm; P=0.25), LVPWd ((5.97±1.16)mm vs (5.72±1.09)mm; P=0.20), DAR ((24.18±3.38)mm vs (24.61±3.51)mm; P=0.49), DAP ((18.26±2.30)mm vs (18.29±2.30)mm; P=0.93), EF ((67.36±4.93)% vs (67.95±5.32)%; P=0.54), and FS ((37.28±3.92)% vs (37.55±4.32)%; P=0.72), respectively. Likewise, no significant differences in RVD, LAD, LVIDs, LVIDd, IVSd, LVPWd, DAR, DAP, EF, and FS were observed between groups 1 and 3 (P>0.05). However, significant differences in LVIDs and LVIDd were found between groups 2 and 3 (P=0.029 and 0.012, respectively).
Sagittal plane Cobb angle
Patients were further classified into three subgroups according to kyphotic Cobb angle: <20° (n=33), 20°-40° (n=78), and >40° (n=104). Analysis of the data similarly showed significant differences in RVD between groups 1 and 2 ((18.27±3.66) mm vs (16.54±3.57)mm; P=0.031), although the parameters were within normal ranges. Groups 1 and 2 had similar cardiac structure and function parameters: LAD ((27.06±3.28)mm vs (26.88±3.63)mm; P=0.84), LVIDs ((25.64±3.33)mm vs (25.29±3.37)mm; P=0.62), LVIDd ((41.06±4.04)mm vs (40.36±4.81)mm; P=0.49), IVSd ((5.74±0.78)mm vs (5.71±1.07)mm; P=0.88), LVPWd ((5.80±1.02)mm vs (5.82±1.13)mm; P=0.94), DAR ((24.82±3.16)mm vs (23.83±3.39)mm; P=0.15), DAP ((18.73±2.31)mm vs (18.19±2.40)mm; P=0.27), EF ((68.01±5.77)% vs (67.77±5.25)%; P=0.82), and FS ((37.48±4.45)% vs (37.55±4.12)%; P=0.94), respectively. There was also a significant difference in DAR between groups 2 and 3 ((23.83±3.39)mm vs (24.90±3.30)mm; P=0.028). No significant differences in RVD, LAD, LVIDs, LVIDd, IVSd, LVPWd, DAP, EF, and FS were found between groups 2 and 3 (P >0.05).
Types of deformity
Parameters reflecting cardiac structure and function were comparable between adolescents with different types of congenital scoliosis, specifically segmentation failure (group 1), formation failure (group 2), and mixed-type failure (group 3). Groups 1, 2, and 3 had similar LAD ((26.95±3.39)mm, (27.56±4.53)mm, and (27.38±4.20)mm), LVIDs ((25.31±3.19)mm, (25.47±3.55)mm, and (24.91±3.22)mm), LVIDd ((40.44±4.52) mm, (40.72±5.41) mm, and (39.74±4.49)mm), IVSd ((5.87±1.02)mm, (5.77±1.00)mm, and (5.74±1.03)mm), LVPWd ((5.90±1.10)mm, (5.81±1.13)mm, and (5.66±1.05)mm), DAR ((24.51±3.41)mm, (24.74±3.58)mm, and (24.18±2.96) mm), DAP ((18.43±2.07)mm, (18.14±2.68) mm, and (18.37±2.02)mm), EF ((67.54±5.11)%, (68.05±5.40) %, and (67.83±4.84)%), and FS ((37.23±3.86)%, (37.59±4.46)%, and (37.55±3.75)%) values, respectively. However, obvious differences in RVD were observed between patients with formation failure and those with mixed-type failure ((17.57±4.13)mm vs (15.99±3.11)mm; P < 0.05).
Cardiac structure and function were compared between male and female patients. The mean LVIDd ((41.83±5.36)mm vs (39.31±4.25)mm; P <0.001), LVIDs ((26.08±3.38)mm vs (24.68±3.20)mm; P=0.002), IVSd ((6.17±1.19)mm vs (5.52±0.77)mm; P <0.001), LVPWd ((6.16±1.27)mm vs (5.54±0.88)mm; P <0.001), and DAR ((25.22±3.76)mm vs (24.01±2.93)mm; P=0.009) values were significantly greater for male than for female patients. RVD, LAD, DAF, EF, and FS were not significantly different between the two groups (P >0.05).
Congenital scoliosis is often associated with intraspinal abnormalities and other organ defects. The embryonic development of the vertebrae is closely related to that of the spinal cord and the organs of the mesoderm.14-18 McMaster17 reported intraspinal abnormalities in 18% of 251 patients who underwent myelography. Guerrero et al19 found genitourinary abnormalities in 34% of patients with congenital scoliosis using ultrasound and intravenous urography. The exact incidence of congenital heart disease associated with congenital scoliosis has not been reported. Hensinger et al20 found a 14% incidence of congenital heart disease among patients with Klippel-Feil syndrome. In our study, 34 patients (15.8%) had intraspinal abnormalities that included tethered cord, low conus, Chiari malformation, diastematomyelia, and syrinx. Only 15 patients (6.98%) had urogenital system deformity. The difference between the results in our study and previously reported studies can be explained by selective bias. To assess the effect of isolated congenital scoliosis on the heart and avoid the inborn abnormality of cardiac structure and function, we selected only patients without congenital heart disease. Consequently, some patients were then excluded from the sample. Furthermore, ultrasound alone was used as the screening method, which might not be as sensitive as the combination of ultrasound and intravenous urography.
The crook and rotation of vertebrae decreases the volume of the thoracic cage and collapses the prothorax on the convex side, which causes a flat back and protrusion of the prothorax on the concave side. Soft tissue structure also changes accordingly. All of these changes not only decrease the volume of the thoracic cavity but also restrict respiratory movement of the ribs, which thus influences cardiopulmonary function.21 Westate and Moe22 reported that vital capacity and maximal ventilatory volume in patients with scoliosis were lower than normal and were significantly correlated with the Cobb angle. Pulmonary function becomes worse as the Cobb angle increases. Theoretically, spinal and thoracic deformities will similarly affect the heart. Therefore, it is assumed that the more severe the deformity of the spine, the worse the effect on the heart.
Ultrasound was used routinely preoperatively to evaluate cardiac structure and function, i.e., to noninvasively measure structural indices of the heart chambers and large vessels, blood flow rate, direction of bloodstream, and quality of bloodstream. EF and FS are indicators of the systolic function of the left ventricle.23 Ultrasound is useful for quantitatively and qualitatively assessing cardiac structure and function.
We found that parameters related to cardiac structure and function were within normal ranges in adolescents with congenital scoliosis, which suggests that spinal development has little influence on cardiac structure and function in this population group. This finding is in contrast with the finding that spinal development does affect pulmonary function. A possible reason for the lack of effect of spinal deformity on cardiac structure and function is the anatomical position and characteristic of the heart: the heart is located in the central area of the thoracic cavity and is not restricted or compressed because of deformities that occur during development. Additionally, the contraction and dilation of the heart are active movements that are not affected by respiratory movement.
Jackson et al24 found that AVR correlated closely with the degree of scoliosis and had the highest correlation with pain of all radiographic findings and deformities studied. However, we found that cardiac structure and function were similar between patients with an AVR ≤I° and those with an AVR >I°.
In a study of 25 patients with congenital scoliosis, Muirhead and Connor25 found a significant correlation between diminished vital capacity and severity of curvature. The mean age of the present study population was 12 years, the mean Cobb angle was 71° (range: 43° to 130°), and the mean forced vital capacity was 67%. In contrast, Day et al26 found normal lung function in 11 untreated patients with congenital scoliosis with a mean age of 11.6 years, whereas the mean Cobb angle of curvature was much smaller—34° (range: 16° to 58°). In order to determine the relation between the scoliotic Cobb angle and cardiac structure and function in our study, the patients were subdivided by the severity of spinal deformity. LVIDs and LVIDd were significantly lower in the group with severe spinal deformity than in the group with moderate spinal deformity. This finding indicates that severe scoliosis may affect the development of the heart, especially that of the left ventricle.
McMaster et al27 reported that an increase in the severity of kyphosis was associated with a significant increase in respiratory impairment. Assuming that the deformity in the sagittal plane may also have an influence on the heart, we found a high RVD in patients with flat back deformity and dilatation of the DAR in patients with kyphosis. Bergofsky et al28, by demonstrating that the wedge pressure and cardiac output were normal, found that pulmonary hypertension in kyphoscoliotic patients was primarily due to an increase in pulmonary vascular resistance. They considered this to be the result of compression and kinking of small vessels in the lungs. Therefore, in our study, changes in the sagittal plane may have resulted in compression and kinking of small vessels in the lungs and peripheral vasculature, which in turn increased blood pressure in the pulmonary artery and aorta. Obviously, prophylactic spinal surgery at an early age was beneficial for these patients.
Basu et al29 reported that the proportion of congenital heart disease was higher in patients with congenital kyphosis (33%) and in those with scoliosis caused by mixed defects (37%). Similarly, in our research, the incidence of RVD was significantly lower in patients with mixed-type failures than in patients with formation failures. The difference in cardiac structure between patients with formation failures and those with mixed-type failures suggests that complex deformities affect the development of the heart more severely than do simple deformities.
The regimen used to identify possible candidates for congenital spinal deformity surgery should routinely include echocardiography. Patients with congenital scoliosis resulting from mixed bony defects and/or a severe scoliotic Cobb angle or deformity in the sagittal plane should also undergo routine echocardiography, because the risk of cardiac structure in these patients is higher than that in the healthy population.
Our research showed no significant difference between the indices related to cardiac function in adolescents with congenital scoliosis. These indices—including AVR, side of the thoracic curvature, Cobb angle in the coronal plane, Cobb angle in the sagittal plane, type of deformity, and sex—have little influence on cardiac function.
Although cardiac structure and function in adolescents with congenital scoliosis were found to be in the normal range, patients with scoliosis in advanced stages usually have clinical signs and symptoms of cardiac dysfunction.6,7,30 It has been hypothesized that cardiac dysfunction in patients with scoliosis in advanced stages is caused by chronic hypoxemia, which leads to pulmonary artery hypertension and decreasing cardiac function.
Unfortunately, because our study was retrospective, we were unable to determine whether the structural changes are caused by geometric changes in the heart. Further research is needed to identify whether these changes persist after correction of spinal deformities.
In conclusion, congenital scoliosis affects cardiac structure, but not cardiac function. The main factors related to cardiac structure abnormalities include convexity, Cobb angle in the coronal and sagittal planes, type of deformity, and sex. Although our conclusion has important implications in terms of patient assessment and counseling, supplementary prospective measurements are required to identify the natural history of scoliosis in the adult life stage.
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