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Neuroradiology |
1 From the Departments of Radiology (R.J.N., T.L., J.T.W., J.M.A.v.E., W.H.B.), Neurosurgery (E.M.J.C.), and Surgery (R.J.N., M.J.J.), Maastricht University Hospital, P. Debyelaan 25, 6202 AZ Maastricht, the Netherlands. Received October 15, 2003; revision requested January 8, 2004; revision received January 27; accepted February 24. Address correspondence to R.J.N. (e-mail: nijenhuis@rad.unimaas.nl).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSION REFERENCES |
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MATERIALS AND METHODS: Eight patients (three men and five women; mean age, 58 years; range, 42–83 years) with a thoracic herniated disk underwent contrast-enhanced MR angiography of the thoracoabdominal aorta and posterior branches. Imaging was performed with three-dimensional first-pass contrast-enhanced MR angiographic technique and a triple dose of gadolinium-based contrast agent. Images were analyzed by two observers in consensus to localize the Adamkiewicz artery (AKA) and its connections to the aorta and the anterior spinal artery (ASA). This information was used to determine any change in surgical approach.
RESULTS: In all eight patients, the AKA, the ASA, and the connections with the aorta were identified. The AKA originated between T9 and L2 in all patients and derived from the left side of the aorta in 75% (six of eight) of the patients. In three patients in whom the AKA was observed on the left side, the surgical approach was changed to the right side to preserve spinal cord integrity.
CONCLUSION: Preoperative imaging of the AKA is feasible with contrast-enhanced MR angiography. Contrast-enhanced MR angiography can be used to image the main feeding arteries of the spinal cord in patients undergoing thoracoscopic spinal surgery, and results can be used to change the side of surgical approach.
© RSNA, 2004
Index terms: Magnetic resonance (MR), vascular studies, 37.12142, 37.12143 • Phantoms • Spinal cord, blood supply, 37.12142 • Spine, intervertebral discs, 32.783
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSION REFERENCES |
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Change of the side (right vs left) of surgical approach has been suggested when preoperative imaging reveals that the main feeding artery of the lower spinal cord (T8 through L2) is in the surgical field (3,4). Nowadays, these surgical procedures are more frequently performed endoscopically with a minimally invasive video-assisted thoracoscopic surgical technique (5,7). During video-assisted thoracoscopic surgery, segmental arteries are frequently damaged or sacrificed to prevent bleeding (8), which could possibly lead to paraparesis or paraplegia. Preoperative imaging of the blood supply system could help in the estimation of the risk for postoperative complications.
The artery that is considered to be primarily responsible for the blood supply to the lower spinal cord is the great anterior radiculomedullary artery, also known as the Adamkiewicz artery (AKA). This artery connects the segmental artery, from which it originates, directly through a typical hairpin configuration to the anterior spinal artery (ASA). Besides the AKA, which is by definition the largest of possibly many smaller radicular arteries, more anterior radicular arteries may arise from segmental arteries at other vertebral levels and also may supply the spinal cord. The vertebral level of the segmental artery, from which the AKA derives, is characterized by substantial interindividual variation. Koshino et al (9) showed that the AKA may originate from the vertebral levels of T5 down to L2.
Because of this variability in anatomy of the lower spinal cord blood supply and the potentially devastating consequences of injury to the blood supply during surgery, it is of direct clinical relevance for the patient to undergo preoperative imaging for visualization of the feeding arterial system of the lower spinal cord. The current standard of reference for visualization of the spinal vasculature is intraarterial digital subtraction angiography (DSA), with selective contrast agent injection into segmental arteries (10). However, intraarterial DSA involves radiation exposure, it requires injection of potentially nephrotoxic contrast media, and most important, it is not without risk with regard to induction of spinal cord ischemia (10). Therefore, intraarterial DSA is not often performed, even though it may yield clinically important information. As an alternative to intraarterial DSA, contrast material–enhanced magnetic resonance (MR) angiography recently has been described for noninvasive imaging of the spinal vasculature in patients with a thoracoabdominal aneurysm (11–13). The lower degree of detection of the AKA with contrast-enhanced MR angiography, however, remains an unsolved problem. This could be due to the absence of this vessel in some patients and the use of a suboptimal MR imaging technique.
Thus, the purpose of our study was to prospectively investigate the feasibility of contrast-enhanced MR angiography for visualization of the spinal vasculature in patients referred for video-assisted thoracoscopic surgical treatment of thoracic herniated disk and to prospectively assess the influence of preoperative imaging of the spinal vasculature on the choice of surgical approach.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSION REFERENCES |
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The ASA, for instance, runs from cranial to caudal direction, which is nearly parallel to the magnetic field. The segmental arteries, on the other hand, run along the vertebrae, perpendicular to the magnetic field. As one looks at the AKA, the first and the last part of this artery are also perpendicularly orientated to the magnetic field. The phantom was slightly (about 5°) tilted with respect to the three orthogonal axes of the MR imaging system to allow signal averaging over many subvoxel positions. Signal-to-noise ratio (SNR) was calculated for each tube diameter. For each tube, signal was measured by one observer (R.J.N.) in a user-defined region of interest that comprised the enhanced parts inside the tubes. These results were used to investigate the relationship between signal level and tube diameter. Regions of interest were drawn after the display of the images was magnified on a graphic workstation (Sun UltraSparc; Sun Microsystems, Sunnyvale, Calif) with commercially available image processing software (Easy Vision, release 4.0; Philips Medical Systems, Best, the Netherlands). All regions of interest had the same length (20 mm) along the tube axes; the sizes (ie, width) of the regions of interest perpendicular to the tube axes increased from 0.1 to 4 mm. Background signal and noise were measured and averaged with a region of interest that was placed between the tubes at different positions in the phantom. The distance between the region of interest and the outer tube wall was approximately 1 mm.
Patient Study
From August 2002 until January 2003, eight patients (three men, five women) who subsequently planned to undergo elective surgical repair of a symptomatic thoracic herniated disk participated in this study. The mean age was 58 years (range, 42–83 years). None of these patients had any history of vascular disease. The institutional review board of the hospital approved the protocol, and written informed consent was obtained from all patients.
Imaging Protocol
All patients underwent MR imaging preoperatively, and MR imaging consisted of three components. Patients were imaged in the supine position. At first, T2-weighted anatomic survey imaging was performed to localize the vertebrae and the course of the spinal cord. Subsequently, a bolus-timing image was obtained to determine the imaging delay. Finally, contrast-enhanced MR angiography was performed. All acquisitions were performed with a phased-array spine coil and a 1.5-T MR imaging system (Philips Intera, release 8; Philips Medical Systems).
The imaging field of view (FOV) covered the fifth thoracic vertebra (T5) down to the fifth lumbar vertebra (L5) to ensure that the AKA was in the FOV. Anatomic transverse and sagittal T2-weighted survey MR images were obtained. Acquisition parameters were 2686/120 and a flip angle of 90°. The truly measured voxel size was 1.25 x 1.67 x 4.0 mm3. When necessary, the study MR imaging was combined with a more elaborate clinical MR imaging, and the combination provided dedicated preoperative information in regard to the herniated disk anatomy.
Synchronization of the sampling of the center of k-space profiles with the peak contrast agent (same as that used in the phantom study) concentration was achieved with injection of a test bolus of 2 mL. From the bolus-timing image, the time between the start of contrast agent injection and maximal enhancement of the distal aorta and segmental arteries was determined by using the dynamic viewing mode of the imaging unit. The test bolus was injected at a speed of 3 mL/sec with a power injector (Spectris; Medrad, Indianola, Pa), and after injection, a saline flush of 25 mL was injected at a speed of 3 mL/sec. The time between the start of injection and total enhancement of the distal aorta was used as the imaging delay in obtaining the subsequent contrast-enhanced MR angiographic image.
To obtain the contrast-enhanced MR angiographic image, a triple dose (0.3 mmol per kilogram body weight) of the contrast agent was injected at a speed of 3 mL/sec, and after injection, a saline flush of 25 mL was injected at a speed of 3 mL/sec. Contrast-enhanced MR angiography was performed with two T1-weighted dynamic phases that each lasted shorter than 40 seconds. This time and the centric k-space filling ensured a difference between the arterial (first phase) and venous (second phase) enhancement. FOV size in the craniocaudal direction (frequency encoding) was 45 cm, and that in the anteroposterior direction (phase encoding) was 16 cm. The number of sections was individually adjusted (range, 70–80) to include the entire vertebral cross section over the total FOV (T5 through L5). The acquisition parameters were as follows: 5.9/1.9; flip angle, 30°. Truly measured voxel size was 0.8 x 0.8 x 1.2 mm3. The k-space was filled by using an elliptic-centric order (CENTRA; Philips Medical Systems). Acquired sections were 1.2 mm thick and were reconstructed to sections of 0.6-mm thickness.
Image Analysis
Images in all patients were evaluated in consensus, with consideration of the level and the side of the AKA by two observers (R.J.N. and J.T.W., with 2 and 5 years of experience in contrast-enhanced MR angiography, respectively).
The contrast-enhanced MR angiographic images were analyzed by using multiplanar reformation and maximum intensity projection of targeted regions at the same graphic workstation and with the same commercially available image processing software as were used for the phantom studies. The transverse and sagittal T2 sections were used for the verification of the vertebral level of the segmental artery that was connected to the AKA.
The targeted maximum intensity projection was generally used for verification of the segmental artery. With multiplanar reformation, it was possible to search the whole spinal cord for vascular structures starting from L5 and moving upward to T5. With transverse sections, the spinal column was systematically (from vertebra to vertebra) screened upward for the bright appearance of the cross section through the AKA and ASA. When this cross section was encountered, a new cross-sectional plane was drawn perpendicular to these two vessels (Fig 1), and a new stack of sections was created with multiplanar reformation. When both structures (cross sections of the ASA and the AKA) were in the same newly created plane, the full length of the AKA became visible.
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In the postoperative course, patients were monitored by the neurosurgeon for paraplegia and bleeding from segmental arteries, which were considered to be major adverse outcomes.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSION REFERENCES |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSION REFERENCES |
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MR Angiography
From a technical point of view, it is very challenging to image the spinal vasculature because it is characterized by ultrasmall vessel diameters less than 1 mm and because the location is variable in the large body region that comprises the entire thorax and abdomen. The diameter of the ASA (0.2–0.8 mm) and of the AKA (0.5–1.2 mm) is characterized by substantial interindividual variation (9,14). The critical diameter of 0.3 mm at which no distinction between artery and surrounding fluid can be made in the phantom is close to the smallest reported diameter at which the ASA may be visualized. This suggests that all the AKAs observed in our patient group are at least 0.3 mm in diameter. The ASA could not be followed all the way from T5 down to L5 in all patients.
Particularly in the high and middle part of the thoracic segments, the ASA was not observed. The ASA has the smallest diameter in this part of the spine and is therefore also most vulnerable to ischemia. According to our phantom study, the diameter of the ASA is expected to be less than 0.3 mm in these segments. Another reason why depiction of the ASA in the high and middle thoracic segments was not achieved is that this area is associated with the most image artifacts caused by heart motion.
Results of our study with consideration of the lateralization (75% left) and level (all between T9 and L2) of the AKA origin are in excellent agreement with findings in literature on vascular anatomy. In a postmortem study in 102 persons, Koshino et al (9) reported a left-sided origin of the AKA in 70%. In 91% of all patients, the AKA arose from a vertebral level between T8 and L1. Bowen et al (14) found that the AKA arose between T9 and T12 in 62%–75% of patients.
In our study, a higher percentage (100%) for detection of the AKA and ASA was found than was previously reported in publications (11–13) about contrast-enhanced MR angiography. Although the number of included patients was limited, several explanations can be given. These are that a larger FOV covering L5 up through T5 was used, that a higher arterial contrast agent concentration was employed, and that there was an absence of gross vascular pathology in the patient population of the study.
In this study, a larger craniocaudal FOV (450 mm) than that used in the studies of Yamada et al (11,12) (FOV, 280–300 mm) and of Yoshioka et al (13) (FOV, 240 mm) was possible with the use of a phased-array (whole) spine coil. This means that a larger body region was investigated to locate the AKA. In our study, spatial resolution was comparable with that in the study of Yamada et al (11,12).
Yoshioka et al (13) achieved a voxel size that was two times smaller with use of a phased-array spine coil, but the FOV they used was almost half the size of the FOV we used. That improved imaging was achieved in our study can also be noted from the additional small vessels that were depicted. In two patients, more than one anterior radicular artery was found, and this artery is by definition thinner than is the AKA. Moreover, in two patients, posterior spinal arteries were observed, which are thinner than is the ASA.
Synchronization of peak arterial contrast agent concentration with acquisition of central k-space profiles is one of the most important aspects of contrast-enhanced MR angiography. When one starts imaging too early or too late, a great deal of signal will be lost. In the current study, an elliptic-centric manner of k-space filling was applied. First, the center of k-space was filled, and this process provided the main signal contrast to the desired vessels. Later, the outer k-space regions were filled, and this process determined the spatial details of the imaged structures. The time of bolus arrival varied within at least 5 seconds among patients, and this variation was sufficiently large to allow degradation of image contrast.
We used the same amount of contrast agent but a faster injection speed (3 mL/sec) than that (0.8–2 mL/sec) used in the study of Yamada et al (11,12). When one compares the injection protocol of Yoshioka et al (13) with that used in our study, one may observe that they used a smaller dose of contrast agent (0.2 mmol/kg) and a far slower injection rate (0.2 mL/sec). Our faster injection speed was chosen to provide a higher first-pass arterial concentration of contrast agent before T2* effects dominated, and thus, these features yielded improved arterial T1 signal. A high bolus concentration fits to the centric k-space filling order and the short acquisition time (less than 40 seconds) to allow separation of arterial from venous enhancement. Slow injection speeds allow longer acquisition times (in the study of Yoshioka et al [13], 5–6 minutes), but they provide angiographic images in which both arteries and veins are equally enhanced. The triple dose of contrast agent in combination with the fast injection rate, as used in the current study, is reported to be safe (16,17).
In our study, another reason for the larger percentage of observed AKAs is that our patients did not have any symptomatic vascular disease or insufficiency. The presence of atherosclerotic plaques may contribute to degradation of visualization of the AKA and ASA, because reduction of the arterial lumen diameter and flow hampers contrast agent arrival.
An alternative modality to MR angiography for visualization of spinal vasculature is computed tomographic (CT) angiography. Kudo et al (18) used CT angiography in patients with known liver disease or in those who were suspected of having it but who did not have vascular pathologic findings. They found that the AKA was visualized in a limited craniocaudal FOV in 13 (68%) of 19 patients. Takase et al (19) used CT angiography and a larger FOV in patients with thoracoabdominal vascular pathologic findings and found this artery in 63 (90%) of 70 patients. Yoshioka et al (13) compared results obtained with CT angiography (24 of 30 patients) and MR angiography (20 of 30 patients) in patients with thoracoabdominal aneurysms and concluded that both techniques are suitable.
Potential Benefit of MR Angiography for Thoracoscopic Microdiscectomy
In thoracoscopic surgery for herniated disk, several factors determine the surgeon’s choice of a left-sided or a right-sided approach. These are as follows: the mediolateral localization of the herniated disk, the vertebral level, the presence of an elongated or dilated aorta covering the left lateral surface, and previous transthoracic surgery that caused pleural adhesions. The choice of the side of approach is also hampered by the presence of anatomic structures such as the liver. Therefore, it is difficult to perform surgery from the right side at T9 and downward. Most thoracic herniated disks occur at these lower thoracic levels and are thus preferentially approached from the left side, where the AKA is most often located.
Segmental vessels are frequently traumatized or sacrificed, and this result leads to a broadening of the surgical field around the pathologically affected disk. This might damage the blood supply to the AKA, which in turn may lead to spinal cord ischemia, when possible collateral circulation fails. Exact knowledge of the segmental feeder level would permit the surgeon to alter his or her surgical strategy whenever necessary. In cases in which the segmental artery that gives rise to the AKA runs over one of the vertebral bodies in the surgical field, it is at risk to be accidentally or even deliberately coagulated during surgery. In three of eight patients (herniated disk at levels T10 through T12), the initially planned approach through the left hemithorax was abandoned, and a right-sided approach was chosen instead. The surgeon thus avoided surgical contact with the AKA feeder. In all three patients in whom the approach was changed, surgery and the postoperative course were uneventful. In the other five patients, the AKA originated above or below the level of the vertebrae that had to be partially dissected, so no alteration of side of approach had to be made.
Limitations
Our results, with consideration of the detectability of the spinal arteries, must be interpreted with caution. First, the number of included patients was small, and results in studies with larger groups of patients are needed to verify our results. Furthermore, our phantom model study does not represent a detailed physiologic situation. Flow effects of the cerebrospinal fluid were not taken into account and may contribute to deterioration of the spatial detection limits. The surrounding tissue of the ASA, the anterior radicular arteries, and the segmental arteries is different and not homogeneous. We used a fluid with T1 of 800 msec (approximately equivalent to muscle tissue) to represent a worst-case situation. Because cerebrospinal fluid surrounds the spinal vessels, the in vivo detection would yield depiction of vessel diameters that could not be seen in the phantom. Use of a T1 representative of cerebrospinal fluid would more closely reflect the surrounding environment of the ASA and would have yielded better detection results for our phantom study but would not have been representative of the anterior radicular arteries and the segmental arteries.
In addition, the concentration of the contrast agent is static in the phantom and does not reflect the bolus dynamics in the arteries. The tube walls (plastic material) yield zero signal contribution in the partial-volume effects, and this result reduces the detected signal in the smaller tubes. The influence of these shortcomings might have diminished our results concerning spatial resolution. The use of a tube with a 0.3-mm diameter, which was not available, represents the crossing between signal of the tube and that of surrounding fluid and is just an indication that vessel diameters smaller than the voxel sizes can be detected. In conclusion, we demonstrated that contrast-enhanced MR angiography aids in the visualization of the feeding arteries of the lower spinal cord and that visualization is important in the preoperative planning of thoracoscopic surgery for herniated disk.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, R.J.N.; study concepts, R.J.N., T.L., M.J.J., J.M.A.v.E., W.H.B.; study design, R.J.N., T.L., E.M.J.C., W.H.B.; literature research, R.J.N.; clinical studies, R.J.N.; experimental studies, R.J.N., W.H.B.; data acquisition, R.J.N., E.M.J.C., W.H.B.; data analysis/interpretation, all authors; manuscript preparation, R.J.N., W.H.B.; manuscript definition of intellectual content, revision/review, and final version approval, all authors; manuscript editing, R.J.N.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSION REFERENCES |
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), and perpendicular, along the 0.6-mm voxel side (
), to the magnetic field. Dashed line represents SNR of surrounding tissue-mimicking fluid. At approximately 0.3-mm tube diameter (0.3-mm diameter not available in this study), SNR of tube contents in both orientations and surrounding fluid are equal.
