The Relation Between Organ Anatomy and Preexistent Vertebral Rotation in the Normal Spine
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The relation between organ anatomy and preexistent vertebral rotation in the normal spine Magnetic resonance imaging study in humans with situs inversus totalis 7 Kouwenhoven JWM Bartels LW Vincken KL Viergever MA Verbout AJ Delhaas T Castelein RM Spine 2007;32(10):1123-28 Introduction Adolescent idiopathic scoliosis (AIS) has been the subject of many studies, however, the pathogenesis of this complex rotational deformity remains little understood.1-12 Scoliosis is a three-dimensional deformity of the spine characterized by deformation in the sagittal (thoracic lordosis), frontal (lateral curvature) and transverse plane (vertebral rotation). A typical feature of scoliosis is the fact that vertebral rotation and the development of lateral curvature are coupled phenomena (i.e., rotation of the vertebral bodies is always directed into the convexity of the lateral curve).13 In AIS, the most prevalent curve types show a primary thoracic curve that is rotated to the right side.1;10;14-18 Although several explanations have been suggested,4;5;8;9;19-25 of which handedness and the anatomy of the thoracic aorta most frequently, the cause of this preferred direction still has to be resolved and remains one of the clas- sical enigmas in orthopaedic surgery. In humans, as well as in quadrupeds, the authors recently demonstrated a pattern of vertebral rotation in the normal, nonscoliotic spine (i.e., the mid and lower thoracic vertebrae showed a predominant rotation to the right side).26;27 This pattern is simi- lar to the most prevalent patterns of rotation in AIS. Apparently, humans and qua- drupedal vertebrates share a common factor that causes this rotation. In both spe- cies, the thoracic organs (heart, lungs and aorta) are asymmetrically situated and in close contact with the vertebral column.22;28 We postulate that this asymmetry may play an important role in the development of this preexistent rotational tendency. Occasionally, individuals have a complete mirror image reversal of the internal body organs, called situs inversus totalis. Situs inversus totalis is a rare anatomic variant with an estimated incidence of only 1 per 20,000 in the general population.29;30 The aim of this study was to analyze vertebral rotation in the normal, nonscoliotic spine of humans with situs inversus totalis to investigate if a pattern of rotation ex- ists opposite of what was found in humans with normal organ anatomy. Further- more, we wanted to establish the role of handedness in this particular population. Subjects and Methods Subjects and Magnetic Resonance Imaging (MRI) This cross-sectional MRI study was performed in 39 persons with a presumed diag- nosis of situs inversus totalis. None of these persons had a history of scoliosis or other spinal pathology. Exclusion criteria were: (1) incomplete situs inversus, (2) congenital or acquired deformation of the spine, (3) history of spinal trauma, and (4) history of spinal surgery or chest surgery. The institutional ethics committee ap- 114 Chapter 7 proved this study, and all persons gave written informed consent for participating in the study. As part of the protocol, all persons were screened for handedness by asking them whether they were right or left handed, and asking them to write down their names. After physical examination, which did not show any signs for scoliosis or other spi- nal deformity, MRI scans of the thorax and abdomen were made in supine position using a 1.5-Tesla MR scanner (Achieva, Philips Medical Systems, The Netherlands). After standard multi-stack survey scans, T2-weighted Turbo Spin Echo (TSE) im- ages were acquired in the sagittal and coronal plane of the spine. These images were used to assess spinal alignment and for planning transverse T2-weighted TSE scans that were used for the actual measurement of vertebral rotation. For each vertebra (T2 to L5), a stack of 6 slices was acquired in the transverse plane of the vertebra. The most important scan parameters were: TR/TE = 1500 ms/100 ms, field of view (FOV) = 188×250 mm², slice thickness = 3 mm (no gap), acquired matrix = 144×256, reconstructed matrix = 192×256, number of signal averages (NSA) = 8, turbo factor = 45. A spine coil was used as a receive coil. For planning of these stacks, both the coronal and the sagittal T2-weighted TSE scans were used. MRI Measurement Method Vertebral rotation was measured in the transverse plane from T2 to L5 using the same measurement method as used in our previous study in humans and dogs.26;27 This method consisted of a semi-automated procedure using an in-house created, interactive computer program to calculate the rotation angle of the vertebrae in a robust and reproducible way. For each vertebra, a single slice of the MRI volume was selected at the center of the vertebral body such that the pedicles were clearly visible.31 The axis of rotation was defined through the Center Of Mass (COM) of the spinal canal. Vertebral rotation was defined as the angle between the longitudi- nal axis of each vertebra and the mid-sagittal axis of the trunk (= reference line). The reference line was defined at level T5 as the line between the COM of the spi- nal canal and the COM of the sternum; the longitudinal axis of each vertebra was defined as the line through the COM of the spinal canal and the COM of the ante- rior half of the vertebral body. After manual segmentation (Figure 1), these points and, subsequently, the rotation angles of the vertebrae were calculated fully auto- matically. The reference line was defined as zero degrees rotation. From a caudal view, counter-clockwise rotation of the vertebrae (rotation of the vertebral body to the right side of the subject) was defined as a positive angle (Figure 1), rotation to the left side (clockwise) as a negative angle (for details see Kouwenhoven et al 2006).26 The relation between organ anatomy and preexistent vertebral rotation in the normal spine 115 Figure 1. Transverse MRI scan at level T5. Longitudinal axis of vertebra T5 (red) represented by the line (green) through the COM of the vertebral canal and the COM of the anterior half of the vertebral body. Reference line (light blue) drawn through the COM of the vertebral canal and the COM of the sternum (dark blue). Because of the radiation dose and its associated health risks, computed tomography (CT) could not be used in this cross-sectional study. For this reason, we used MRI, which does not involve ionizing radiation. The switch from CT to MRI demanded a re-evaluation of the reliability of our method. Therefore, three different observers manually segmented the slices of T2-T6 in the same four randomly chosen subjects independently. For the intraobserver analysis, Observer 1 manually segmented these slices three times at separate sittings. Statistics Statistical analysis was performed by means of SPSS statistical software, version 12.0.1 (SPSS, Inc., Chicago, IL). The observed frequencies of right and left verte- bral rotation were used to test the null hypothesis of equal probability with the bi- nomial test. To determine if the mean vertebral rotation angles were statistically sig- nificant, we used the one-sample T test. A P-value of less than 0.05 was considered to be statistically significant. 116 Chapter 7 Results Evaluation of the MRI images showed that all persons had a normal spinal align- ment in the frontal and sagittal plane, without congenital or acquired spinal defor- mities. It, however, also revealed that 2 persons where found to have an incomplete situs inversus and, therefore, had to be excluded from this study. Table 1. Right-left distribution of vertebral rotation (T2-L5). Vertebra Direction of rotation P Right Left T2 27 (73%)* 10 (27%)* 0.008 T3 27 (73%)* 10 (27%)* 0.008 T4 21 (57%) 16 (43%) 0.511 T5 11 (30%)* 26 (70%)* 0.020 T6 6 (16%)* 31 (84%)* <0.001 T7 6 (16%)* 31 (84%)* <0.001 T8 9 (24%)* 28 (76%)* 0.003 T9 11 (30%)* 26 (70%)* 0.020 T10 13 (35%) 24 (65%) 0.099 T11 12 (32%)* 25 (68%)* 0.047 T12 17 (46%) 20 (54%) 0.743 L1 19 (51%) 18 (49%) 1.000 L2 20 (54%) 17 (46%) 0.743 L3 22 (59%) 15 (41%) 0.324 L4 23 (62%) 14 (38%) 0.188 L5 23 (62%) 14 (38%) 0.188 Right-left distribution of vertebral rotation at T2-L5 in the normal, nonscoliotic spine of 37 persons with SIT. The observed frequencies of right and left vertebral rotation at each level are given along with the significance level. * The observed frequencies differ significantly from an equal right-left distribution (P<0.05). The relation between organ anatomy and preexistent vertebral rotation in the normal spine 117 Vertebral rotation was analyzed in the group of 37 persons who had a complete situs inversus. This group consisted of 20 males and 17 females, with a mean age of 32.1 years (range 7-74 years). Thirty-two persons were right handed (86%), and 5 were left handed (14%). There were no persons who were ambidextrous. Analysis of the data showed a predominant rotation to the left side of the mid and lower thoracic vertebrae (T5-T12). The observed frequencies of right and left ver- tebral rotation differed significantly from an equal right-left distribution at levels T5-T9 and at level T11 (P<0.05). The upper thoracic (T2-T4) and lumbar verte- brae (L1-L5) showed a predominant rotation to right side, with significant values at levels T2 and T3 (P<0.01) (Table 1). Measurement of the angles of vertebral rotation showed a mean rotation angle to the left side of the mid and lower thoracic vertebrae.