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1
Department of Radiology, Guy's Hospital, Guy's and St. Thomas' Hospital Trust,
St. Thomas St., London SE1 9RT, United Kingdom.
2
Department of Radiological Sciences, Guy's Hospital, Guy's and St. Thomas'
Hospital Trust, London SE1 9RT, United Kingdom.
3
Department of Nephrology and Transplantation, Guy's Hospital, Guy's and St.
Thomas' Hospital Trust, London SE1 9RT, United Kingdom.
Received September 28, 2000;
accepted after revision February 12, 2001.
Address correspondence to S. C. Rankin.
Abstract
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MATERIALS AND METHODS. Eighty consecutive potential living kidney donors were investigated. Fifty patients underwent CT angiography and 30 underwent MR angiography before donor nephrectomy. CT was performed using 3-mm collimation with a pitch of 1.6 after the injection of 150 mL of nonionic contrast medium. The axial data, multiplanar reconstructions, and maximum intensity projections were reviewed. MR angiography was performed on a 1-T magnet using a contrast-enhanced three-dimensional gradient echo technique. Maximum intensity projections and axial reformations were reviewed. Imaging findings were compared with the surgical results in 54 patients.
RESULTS. CT angiography and MR angiography were 100% sensitive in identifying the main renal arteries and renal veins. CT angiography visualized 37 of the 40 arteries identified at surgery, for a detection rate of 93%. MR angiography visualized 18 of the 20 arteries identified at surgery, a detection rate of 90%.
CONCLUSION. CT angiography and MR angiography are suitable for the noninvasive investigation of living kidney donors and provide all the information required by the surgeon. Both methods may miss small accessory renal arteries. MR angiography does not use potentially toxic contrast material or radiation and is the preferred investigation, with CT angiography reserved for patients unable to tolerate MR imaging.
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The development of helical CT angiography as a noninvasive method of investigating the arterial system is challenging the use of intraarterial digital subtraction angiography for the assessment of the renal arteries. CT angiography is now being replaced in some instances by contrast-enhanced MR angiography, which has the advantage of using a nontoxic contrast medium and no radiation. CT angiography and MR angiography can identify the renal arterial and venous systems on a single study, and either abdominal radiography or MR urography can be performed to assess the calices and ureters at the same visit. Using either CT angiography or MR angiography may allow the noninvasive investigation of the complete renal tract to be performed during a single outpatient visit, with a consequent decrease in patient time and cost. The limitations of these procedures are the difficulties in identifying intrinsic arterial disease and in assessing small vessels.
The purpose of this study was to compare first CT angiography and then MR angiography with the results of surgery to assess whether adequate preoperative information could be provided to the surgeons by these noninvasive investigations.
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CT Protocol
All CT scans were obtained using an AVS 8000 scanner (Philips Medical
Systems International, Best, The Netherlands). No oral contrast medium was
given. A scout image was obtained, followed by acquisition of a volume of data
without contrast medium, using 10-mm collimation with a pitch of 1, from the
diaphragm to the mid pelvis. These data were used to assess any renal
calcification or obvious abnormality that would preclude nephrectomy and to
identify the scaning range for contrast-enhanced images.
The contrast-enhanced scans were obtained using 3-mm collimation with a table feed of 5 mm (pitch of 1.67) from the level of the celiac axis to 2 cm below the aortic bifurcation, or to 2 cm below the lower pole of the lowest kidney, whichever was more inferior. A 300-mm field of view and a 512 x 512 matrix with a reconstruction index of 2 mm were used. One hundred fifty milliliters of nonionic contrast material (300 mg I/mL of iopromide; Ultravist, Schering Health Care, Burgess Hill, UK) was injected at 3 mL/sec through a 20-gauge cannula into the antecubital fossa with a fixed delay of 30 sec between the start of the injection and the initiation of the data collection. The long delay was used because we knew some of the patients would be quite old, with the possibility of a decreased cardiac output, and we wanted a standardized method of scanning. The relatively slow injection rate meant that high levels of contrast enhancement were maintained despite the long delay. The scans were obtained during suspended inspiration after hyperventilation.
Immediately after the acquisition was completed, the patient underwent conventional abdominal radiography to assess the calices and ureters.
Postprocessing of CT Data
The helical axial data were reconstructed with a 2-mm overlapping
reconstruction. The data were transferred to a workstation and curved
multiplanar reconstructions were generated using the axial, coronal, and
sagittal data, and were viewed in the coronal and oblique planes oriented
along the line of the renal arteries. Maximum intensity projections were also
generated after the removal of all areas of high attenuation from the volume
by segmentation. The postprocessing took 20-30 min. All the processing was
undertaken by either the radiology fellow or the attending radiologist.
MR Imaging Protocol
All the MR scans were obtained with a 1-T MR system (Siemens, Erlanger,
Germany) using a phased array body coil. Each acquisition was obtained during
suspended inspiration. No patient preparation was required.
MR angiography was performed using a coronal three-dimensional (3D) fast low-angle shot (FLASH) acquisition (TR/TE, 6.4/2.4; flip angle, 25°). A slab thickness of 80 mm positioned to include the aorta, the kidneys, and the renal arteries, with an effective slice thickness of 2 mm interpolated to 1 mm, a 320- mm field of view, and a matrix of 150 x 256 was used with partial k-space sampling. The center of k-space is located three eighths through the acquisition time. A double dose of gadopentetate dimeglumine (0.2 mmol/kg of Magnevist; Schering Health Care) was injected by hand as rapidly as possible for angiography. The timing of the data acquisition to obtain optimal visualization of the renal arteries was based on a test dose of gadolinium. This test imaging was performed using a single-slice axial turbo FLASH (8.5/4; flip angle, 10°) sequence with the slice positioned just below the origin of the renal arteries. Thirty slices, each 10-mm thick, were obtained in a single position during 30 sec. Two milliliters of gadolinium diluted in saline to the same volume as would be used in the final acquisition was injected by hand through a 20-gauge cannula positioned in the antecubital fossa (estimated rate of injection, 2 mL/sec).
MR venography was performed by repeating the 3D FLASH sequence 60 sec after the final injection of contrast medium to obtain maximal renal vein and inferior vena cava enhancement. Unenhanced and contrast-enhanced axial two-dimensional FLASH sequences (130/6.5; flip angle, 80°) with a slice thickness of 8 mm, a 2.5-mm interslice gap, and an 18-sec breath-hold were used to assess the renal parenchyma.
The calices and ureters were also studied using MR urography (Fig. 1A,1B,1C,1D). Four sequences were used in this assessment: coronal 80-mm half-Fourier acquisition single-shot turbo spin-echo (HASTE) sequences acquired in 7 sec (TE, 1100); coronal multislab segmented turbo spin-echo T2-weighted sequences (TE, 87) with 13 slices of 5 mm each measured in 19 sec; coronal 3D FLASH (TR/TE, 6.4/2.4; flip angle, 25°) sequences performed 5 min after the test injection of 2 mL of gadopentetate dimeglumine diluted in saline, with an 80-mm slab imaged with 40 partitions in 30 sec and interpolated to 80 partitions during reconstruction. The fourth sequence consisted of the third sequence repeated 5 min after the double dose of contrast material used for the final MR angiography. The field of view used was 300-320 mm. The complete renal examination took about 30-40 min.
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Postprocessing of MR Data
The data were transferred to a workstation and the images were processed by
subtracting the unenhanced volume from the contrast-enhanced MR angiogram, MR
urogram, and MR venogram. A freehand region of interest and maximum intensity
projections were used for processing the subtracted MR angiograms and MR
urograms. Multiplanar reformations were used to further process the MR
angiograms and MR venograms using the axial plane. The postprocessing took
about 30 min and was performed by either the radiology fellow or the attending
radiologist.
Data Interpretation
The CT and MR data, including the multiplanar reformations and maximum
intensity projections, were reviewed by two radiologists, both of whom
specialized in cross-sectional imaging; and a consensus view was reached. The
parameters studied included the number and origin of renal arteries, the
presence of early branching arteries, and any intrinsic renal artery disease.
The number of veins and venous anomalies was also noted, as were other renal
or extrarenal disorders. The abdominal radiography performed after the CT was
used to assess the calices and ureters.
Correlation
The surgeon was aware of the CT angiography and MR angiography results and
used this information to guide surgery. The kidney with the least complex
vascular anatomy was chosen preferentially. In the absence of any anatomic
contraindication, the left kidney was usually chosen for donor nephrectomy.
The surgery was performed by one of two experienced transplantation surgeons
using a lateral oblique incision below the twelfth rib with an extraperitoneal
approach, and the ureters were ligated at the pelvic brim. No laparoscopic
surgery was undertaken. The surgeon noted at nephrectomy the number of renal
arteries and veins and the presence of accessory arteries, but could not
assess intrinsic renal artery disease. The surgical data were obtained from
the operative notes written immediately after the surgery and were collected
before the patient was discharged. These findings were then correlated with
the preoperative imaging.
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CT Angiography
The main renal artery was identified in each kidney (100 kidneys).
Seventy-three kidneys had a single renal artery, 24 kidneys had two renal
arteries, and three kidneys had three renal arteries each. Accessory arteries
were better shown on the axial multiplanar reformations than on the maximum
intensity projections (Fig.
2A,2B,2C,2D).
Only three patients underwent conventional intraarterial digital subtraction
angiography, which confirmed the number of arteries (four in one patient and
two in the other two patients) identified on CT angiography.
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Thirty-six patients in this group have undergone nephrectomy. The left kidney was used in 24 patients and the right in 12. In three of the patients accessory arteries were missed on CT angiography. One could not be identified even in retrospect and was a lower pole artery supplying approximately 5% of function, but the artery was successfully anastomosed. One study was technically unsatisfactory and the accessory artery was ligated. In the third instance, which occurred early in our series, the accessory artery was visible in retrospect, supplied 20% of function, and was successfully anastomosed at surgery.
Early branching renal arteries within 1 cm of the origin were identified in seven kidneys on preoperative imaging (Fig. 3).
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We maintained a high index of suspicion for renal artery disease, and angiography was performed if any doubt existed. In one patient, intrinsic renal artery disease with a plaque near the renal artery origin was suspected on CT angiography but was not confirmed on subsequent angiography.
On CT angiography, the main renal vein was identified in 100 kidneys. Ten kidneys had double veins and one had a retroaortic vein. At nephrectomy, the double veins were confirmed in two patients; unsuspected accessory renal veins were found in two patients and were ligated.
The abdominal radiography performed at the end of the CT examination was adequate for the visualization of the calices and ureters, and no significant abnormalities were identified either on imaging or at surgery.
In eight patients, intrarenal abnormalities were identified that included renal cysts (n = 6) and renal scarring (n = 2). Extrarenal abnormalities were seen in five patients and included splenic artery aneurysm (n = 2), hepatic cyst (n = 1), hepatic hydatid cyst (n = 1), and splenomegaly (n = 1).
MR Angiography
The main renal artery was identified in each kidney (60 kidneys).
Forty-five kidneys had a single renal artery, 14 kidneys had two renal
arteries each (Fig. 4), and
one kidney had four renal arteries.
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Eighteen patients in this group underwent nephrectomy. The left kidney was used in 12 patients and the right in six. Accessory arteries were missed on MR angiography in two patients. One accessory artery was a lower pole artery supplying approximately 5% of function that could not be identified even in retrospect. In the other patient, who was the second patient investigated in this group, the accessory artery was visible in retrospect lying immediately behind the renal vein. This case showed the importance of creating axial multiplanar reformations from the original data set in addition to the maximum intensity projections (Fig. 5A,5B,5C), because the accessory vessels are then easier to identify with certainty. We now always create multiplanar reformations. In both these patients the accessory arteries were successfully anastomosed at surgery. Early branching renal arteries were seen in five kidneys on MR angiography. No intrinsic arterial disease was identified.
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On MR venography, the main renal vein was identified in 60 kidneys. Six kidneys had double veins and two had a retroaortic vein. The retroaortic vein was confirmed at donor nephrectomy in one patient (Fig. 6A,6B).
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MR urography gave satisfactory results and required no patient preparation. Unlike Low et al. [1], we performed MR urography without prior hydration, diuretics, or compression pads. The ureters were not always seen in their entirety, but the combination of all four sequences allowed adequate visualization of the calices and at least part of the ureters. The four sequences were used initially as part of a concurrent study in order to identify the most appropriate sequences. Comparing the four sequences, we found the optimal sequence for the calices was the 3D FLASH sequence performed after the test dose, followed by the turbo spin-echo T2-weighted sequence. The use of these two sequences combined increased the visualization of the calices [2].
Renal cysts were identified in four patients, and multiple hepatic cysts in another patient.
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Renal angiography has some potential risks, although the complications are markedly reduced with the use of small catheters in association with digital subtraction angiography [5]. CT angiography, which is noninvasive, has been used for the assessment of renal artery stenosis and living kidney donors [6,7,8,9,10,11,12,13,14,15] with good results, but the ideal would be to replace CT angiography with MR angiography, because MR angiography uses no radiation and the contrast material is less toxic.
Our study was undertaken to compare the results of CT angiography and MR angiography with surgical findings to see if adequate preoperative information could be obtained by these noninvasive methods.
CT angiography was performed using a modification of the final protocol suggested by Platt et al. [13]. Our delay time was chosen as 30 sec because the age range of our patients was variable (28-72 years; mean, 46 years), and the injection rate was decreased to 3 mL/sec to ensure contrast medium levels were adequate throughout the examination. Only one study was technically unsatisfactory, and that study was related to body habitus; in that patient an accessory artery was missed.
A limitation of our study is the lack of angiographic correlation, which could mean that intrinsic renal artery disease may have been overlooked, but CT angiography has been established as being both sensitive and specific for the identification of significant (>50%) renal artery stenosis in the main renal arteries [6,7,8,9,10]. The early studies by Galanski et al. [8] using axial images, multiplanar reformations, and maximum intensity projections found CT angiography had an overall sensitivity of 95% and was 100% sensitive and 92% specific for stenosis greater than 50%. Axial images were the most useful, and maximum intensity projections were helpful for ostial stenosis. Beregi et al. [7] found CT angiography to be 100% sensitive and 98% specific for main renal artery stenosis, but it missed two lesions on distal branches less than 2 mm in diameter. CT angiography may be of limited value in the diagnosis of fibromuscular hyperplasia, particularly in early disease, although Beregi et al. [16] identified 33 of the 38 lesions seen on digital subtraction angiography in 20 patients using CT angiography.
Limited spatial resolution means small arteries of less than 2 mm may not be identified and accessory arteries may be missed. Cochran et al. [12] missed three accessory arteries that were visible in retrospect, but angiography may also miss accessory arteries in up to 8% of patients [12]. We missed three accessory arteries: one could not be identified, one was in a technically suboptimal examination, and one was visible in retrospect. The correlation of this study is with surgery and not with angiography, which will lead to surgical bias because the surgeon will choose the kidney with the least complex vascular anatomy. However, the incidence of accessory and early branching arteries and venous anomalies in our series corresponds with other published data that have angiographic correlation (Table 2).
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In the three patients in our series who had both CT angiography and intraarterial angiography, the number of renal arteries was correctly identified, and the possibility of intrinsic renal artery disease suspected on CT angiography was dismissed.
In our institution, we changed to MR angiography after it had become established as a clinical tool for the assessment of the renal arteries, and after the transplantation surgeons gained experience with it. Contrast-enhanced MR angiography has advantages over both CT angiography and digital subtraction angiography. There is no radiation, the gadolinium has low nephrotoxicity, and a bolus of 0.2 mmol/kg is sufficient to see blood bright against fat. Multiple projections can be obtained, which is an advantage compared with digital subtraction angiography. Contrast-enhanced MR angiography can be combined with other MR techniques to assess the collecting system, renal size, cortical thickness, and parenchymal enhancement [17].
Again, we have no angiographic correlation for our data, but the published results of MR angiography compared with digital subtraction angiography for renal artery stenosis are now satisfactory, with reported sensitivity and specificity for stenosis of the main renal arteries of 93-100% and 92-98%, respectively [18,19,20,21,22]. The results for accessory arteries are not as good because of limited spatial resolution that is not sufficient for intrarenal vessels, segmental arteries, or accessory arteries smaller than 3 mm in diameter. However, new elliptic centric order phase encoding for k-space will provide increased contrast and an increased signal-to-noise ratio and will thus improve small-vessel depiction, and the development of faster gradients will improve resolution and the signal-to-noise ratio [23,24,25]. Korst et al. [26] missed four of 17 accessory renal arteries, of which three were seen in retrospect, but they identified all patients with significant renal artery stenosis of 50-90%. Bakker et al. [21] identified 21 of 22 accessory renal arteries, but that study incorrectly suggested significant stenosis in five renal arteries. However, the negative predictive value and sensitivity were 100%; therefore, MR angiography can be used to exclude significant renal artery stenosis. Fibromuscular hyperplasia may also be difficult to diagnose with MR angiography, especially if a pixel size that is large relative to the vessel size is used, so an imaging slice thickness of less than 2 mm is required for renal MR angiography [27].
Although two-dimensional and 3D reconstructions are helpful for showing vascular anatomy, we found, as did other authors [8, 28], that the axial images in both CT and MR angiography were the most important for the visualization of accessory arteries and early branching arteries (Figs. 2A,2B,2C,2D, 3, and 5A,5B,5C). Therefore, it is important to reconstruct axial multiplanar reformations of the MR imaging data and review these reformations. We missed one accessory artery early in the MR study when we did not reconstruct multiplanar reformations, and in two other (later) patients the accessory artery was identified only on the axial multiplanar reformations. It is also important to review the images directly on the workstation rather than as hard-copy images so that individual arteries can be followed in their entirety to confirm their origin and site of insertion into the kidney. This process is particularly required for vessels arising from the iliac arteries and for differentiation of mesenteric and lumbar vessels from accessory renal arteries.
The results of our study suggest that both CT angiography and MR angiography produce sufficient information about the vascular anatomy for our transplantation surgeons before kidney donation from living donors. Although small accessory arteries may be missed, when found they can usually be anastomosed at surgery; or if they supply only a small amount of renal substance, they may be ligated. Advances in CT technology using multiple detector helical angiography will improve image quality with faster acquisition, narrower effective slice thickness, and improved longitudinal resolution. A decrease in the amount of contrast medium used will also be possible [29]. CT angiography will show both renal and extrarenal disorders that may influence surgery. MR imaging will reveal renal pathology but not all extrarenal disease. A further limitation of MR angiography is the inability to identify calcification in the kidney, but because all our donors undergo sonography before their further investigation, this is not perceived as a problem. Visualization of the calices and ureters is satisfactory using both methods. Rather than use all the four sequences we used in this initial MR imaging study, the number of sequences could be reduced to either 3D FLASH performed after the test dose followed by the turbo spin-echo T2-weighted sequence, or the sequence after the test dose alone [2].
The major limitation of this method of investigation is the potential intrinsic renal artery disease that may be missed. In a recent study by Neymark et al. [30] reviewing 716 preoperative angiograms of living donors, the incidence of renovascular abnormalities was 10%, with fibromuscular hyperplasia occurring in 6.6% of patients. Most of the abnormalities were minimal or mild stenoses. Despite the renovascular abnormalities found, 53% of this group were considered suitable for donation, but the kidney selected was influenced by the angiographic findings. Unfortunately, those authors did not relate whether the patients had been followed up or state the findings in either the donors or the recipients to ascertain whether their low threshold for abnormality was actually appropriate.
In conclusion, despite the lack of angiographic correlation that may have altered surgical management, our surgeons believed both CT angiography and MR angiography provided sufficient information before donation by a living donor. MR angiography is the investigation of choice, with CT angiography being used in patients for whom MR imaging is contraindicated. Intraarterial angiography is reserved for those in whom the noninvasive investigation is either nondiagnostic or suggests an intrinsic vascular abnormality that requires further assessment.
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