Original Research
Genitourinary Imaging
July 23, 2015

Utility of MRI in the Characterization of Indeterminate Small Renal Lesions Previously Seen on Screening CT Scans of Potential Renal Donor Patients

Abstract

OBJECTIVE. The purpose of this study was to determine whether MRI could more confidently characterize indeterminate small renal lesions (< 15 mm) previously seen on CT scans of potential renal donor patients and whether such characterization could impact surgical management and donor candidate status.
MATERIALS AND METHODS. After dedicated contrast-enhanced renal CT examinations of a population of renal donor patients identified indeterminate small renal lesions (< 15 mm), dedicated renal MRI examinations were performed for 55 of those patients. Two radiologists used consensus reading of established MRI characteristics to characterize indeterminate small lesions as simple cysts, hemorrhagic cysts, angiomyolipomas, or solid renal masses.
RESULTS. A total of 94 indeterminate small renal lesions were detected on CT. MRI was able to confidently diagnose 93 of those lesions, including 83 cysts, eight hemorrhagic cysts, and two angiomyolipomas. MRI directly affected the surgical management of four of the patients (7%).
CONCLUSION. For potential renal donor patients, MRI can be an effective means of characterizing lesions that are deemed to be too small to characterize by CT. MRI can also potentially alter the surgical management and donor status of this group of patients.
A kidney from a living donor is the best transplantation option for eligible patients with end-stage renal disease because it offers superior recipient and graft survival, compared with a kidney obtained from a deceased donor [1]. MDCT provides accurate preoperative evaluation of potential kidney donors [24]. Subcentimeter hypodense lesions are common in the kidneys of potential adult donors. On CT, such lesions are difficult to characterize accurately because they are susceptible to volume averaging and pseudoenhancement [57]. When encountered during routine CT examinations of adult patients, such lesions are frequently referred to as hypodensities that are too small to characterize, and they are generally presumed to be benign; follow-up imaging or further characterization is generally not done [7, 8]. However, characterization of such lesions in potential renal donor patients is important to transplant surgeons because potential identification of a solid renal mass in a kidney can significantly affect the donor status of the patient. Therefore, for such patients, further evaluation with MRI may be prudent. Given these considerations, at our institution lesions smaller than 15 mm that are detected on CT examination of potential living renal donor patients but are incompletely characterized are further evaluated using dedicated renal MRI. MRI has shown promise in characterizing small lesions that are not fully characterized by CT examination of other organs, such as the liver, and it has the potential to definitively characterize indeterminate small renal lesions [911].
To our knowledge, no study to date has evaluated the role and influence of MRI in characterizing small renal lesions seen on CT examination of potential renal donor patients. We thus sought to retrospectively determine whether MRI could provide for these patients a more confident characterization of indeterminate small renal lesions (< 15 mm) than that provided by CT and whether such characterization could affect surgical management and donor candidate status.

Materials and Methods

Subjects

The institutional review board at the University of California Davis Medical Center approved this retrospective HIPAA-compliant study. From July 2004 to July 2014, we retrospectively queried our electronic radiology database to identify dedicated renal MRI examinations that included the terms “renal donor,” “kidney donor,” “living related,” “living donor,” and “live donor” in the radiology report. The database search identified a total of 58 renal donor patients. For each of these patients, our PACS database was searched for dedicated renal donor CT examinations that had been performed before the MRI examinations. Three of the 58 patients who were identified were excluded from the study, including one patient who had not previously undergone CT examination, one patient who vomited after the arterial phase and for whom no nephrographic phase images were obtained, and one patient who did not have a nephrographic phase image obtained for an unstated reason. Thus, our study comprised a total of 55 consecutive renal donor patients with dedicated renal CT and MRI examinations. All 55 renal donor MRI examinations were performed to evaluate an indeterminate renal lesion smaller than 15 mm that was seen on renal donor CT examinations.

MDCT Protocol

Because examinations were conducted over a 10-year period, CT examinations were performed using a variety of MDCT scanners, including 4-MDCT (HiSpeed, GE Healthcare), 16-MDCT (LightSpeed, GE Healthcare), 64-MDCT (VCT, GE Healthcare; Sensation and Definition-DS, Siemens Healthcare), and 128-MDCT (Definition-AS, Siemens Healthcare). However, all examinations involved triphasic imaging of the kidneys, including imaging performed during the unenhanced phase, followed by contrast-enhanced imaging of the abdomen performed during the arterial and nephrographic phases, with the use of 100–125 mL of iohexol (Omnipaque-350, GE Healthcare) injected at a rate of 4.0 mL/s. The arterial phase image was acquired using automated bolus triggering that was optimized to acquire images in the phase of peak arterial enhancement in the midabdominal aorta at the level of the kidneys. The corticomedullary phase image was acquired at a fixed scan delay of 55 seconds after completion of the arterial phase. Images from all phases were obtained at a tube voltage of 120 kVp, with a variable tube current–exposure time product using automated tube current modulation, and with a variable pitch. Images in all phases were reconstructed at a thickness and interval of 5.00 mm. In addition, in some patients images were also reconstructed at a thinner thickness, which ranged from 1.0 to 2.5 mm, depending on scanner type.

MRI Protocol

All patients were instructed to fast for 4 hours before MRI examination. Images were acquired using a 1.5-T MRI system (Signa HDxt, GE Healthcare) equipped with a phased-array torso coil for signal reception. The imaging protocol varied because the examinations were conducted over a 10-year period; however, all of the examinations included the following sequences: a coronal single-shot fast spin-echo sequence (FOV, 42 cm; slice thickness, 4–5 mm; spacing, 5–6 mm; TR/TE, 1007.2/89.3; flip angle [FA], 90°; matrix, 384 × 160), a transverse single-shot fast spin-echo sequence (FOV, 40 cm; slice thickness, 4–5 mm; spacing, 5–6 mm; TR/TE, 760.1/89.0; FA, 90°; matrix, 384 × 160), a transverse fat-saturated fast spin-echo T2-weighted sequence (FOV, 40 cm; slice thickness, 4–5 mm; spacing, 5–6 mm; TR/TE, 2000/91.8; FA, 90°; matrix, 256 × 192), a trans-verse unenhanced T1-weighted 2D spoiled gradient-echo sequence performed in phase and out of phase (FOV, 40 cm; slice thickness, 5 mm; spacing, 6 mm; TR/TE [in phase], 140.0/2.2; TR/TE [out of phase], 140.0/4.4; FA, 90°; matrix, 256 × 224), a transverse unenhanced T1-weighted 3D spoiled gradient-echo pulse liver acquisition with volume acquisition sequence (FOV, 36 cm; slice thickness, 5.0 mm; spacing, 2.5 mm; TR/TE, 3.2/1.4; FA, 12°; matrix, 384 × 224). Then, 0.01 mmol/kg of gadodiamide (Omniscan, GE Healthcare) was injected at 2 mL/s, and transverse liver acquisition with volume acquisition sequences were obtained during the arterial and nephrographic phases with the use of the same parameters outlined above. Subtraction images were also generated.

Lesion Characterization

Two board-certified radiologists who specialized in abdominal imaging and who had 2 and 5 years of postfellowship experience reviewed the CT and MRI examinations. They used consensus reading to determine image quality and to identify renal lesions that met the study criteria. The maximal diameter of each lesion was measured using the thinnest CT slices available, and ROIs were placed over the lesion on both unenhanced and contrast-enhanced images, to include two thirds of the lesion. CT definitions of renal lesions were based on definitions found in a publication by Silverman et al. [7]. Lesions that enhanced greater than 20 HU were categorized as enhancing lesions and were deemed to be solid renal masses, whereas those that enhanced less than 10 HU were categorized as nonenhancing lesions. Fluid-density lesions (CT attenuation, 0–20 HU) that did not show enhancement on unenhanced CT examinations were determined to be simple cysts. High-density lesions (CT attenuation, > 20 HU) that did not show enhancement on unenhanced CT images were classified as hyperattenuating (proteinaceous or hemorrhagic) cysts. Lesions containing gross fat (CT attenuation, < −20 HU) were categorized as benign angiomyolipomas. Lesions were characterized as indeterminate if they were smaller than 15 mm, did not meet simple fluid or fat density criteria on unenhanced CT, had indeterminate enhancement (CT attenuation, 10–20 HU), or were too small to identify on unenhanced images and therefore could not be assessed for enhancement.
Both T2 signal and enhancement characteristics of the lesions were taken into account during MRI characterization of the lesion. Subtraction techniques were used to evaluate lesion enhancement. Enhancement was defined as a subjective internal signal intensity in the lesion that was greater than the background noise on subtraction images. A lesion that showed enhancement, regardless of T1 and T2 signal characteristics, was categorized as a solid renal mass. A lesion with markedly high signal on T2-weighted images, low signal on T1-weighted images, and no enhancement was characterized as a simple cyst (Fig. 1). A lesion with high signal on fat-suppressed T1-weighted images but with no demonstrable enhancement was labeled as a proteinaceous or hemorrhagic cyst (Fig. 2). A lesion for which MRI showed features of gross fat, including high signal on T2-weighted images, loss of signal on fat-suppressed images, or signal loss at the interface of the lesion with normal adjacent parenchyma on opposed-phase imaging using the India-ink artifact, was classified as an angiomyolipoma [12] (Fig. 3). A lesion for which opposed-phase imaging showed complete dropout of signal was deemed an indeterminate lesion, because this characteristic may be seen in association with both angiomyolipomas and clear cell renal cell carcinomas [7].
Fig. 1A —58-year-old woman with simple renal cyst.
A, Axial CT nephrographic phase image shows 4-mm renal lesion (arrow) in left inferior pole that is too small for Hounsfield unit measurements of CT attenuation for characterization to be reliably obtained.
Fig. 1B —58-year-old woman with simple renal cyst.
B, Follow-up MR image shows lesion (arrow) with fluid intensity on axial fat-saturated T2-weighted sequence.
Fig. 1C —58-year-old woman with simple renal cyst.
C, Follow-up MR image shows lesion (arrow) with hypointensity on axial unenhanced T1-weighted liver acquisition with volume acquisition sequence.
Fig. 1D —58-year-old woman with simple renal cyst.
D, Follow-up MR image shows lesion (arrow) with no enhancement on axial contrast-enhanced subtracted T1-weighted sequence.
Fig. 2A —22-year-old man with proteinaceous or hemorrhagic cyst.
A, Axial CT nephrographic phase image shows 10-mm indeterminate right renal lesion (arrow) with attenuation of 38 HU.
Fig. 2B —22-year-old man with proteinaceous or hemorrhagic cyst.
B, Renal MR image shows lesion (arrow) with fluid intensity on axial fat-saturated T2-weighted sequence.
Fig. 2C —22-year-old man with proteinaceous or hemorrhagic cyst.
C, Renal MR image shows lesion (arrow) with hyperintensity on axial unenhanced T1-weighted liver acquisition with volume acquisition sequence.
Fig. 2D —22-year-old man with proteinaceous or hemorrhagic cyst.
D, Renal MR image shows lesion (arrow) with no enhancement on axial contrast-enhanced subtracted T1-weighted sequence.
Fig. 3A —28-year-old woman with renal angiomyolipoma.
A, Axial CT nephrographic phase image shows indeterminate 4-mm hypodense lesion (arrow) in inferior right kidney that is too small for Hounsfield unit measurements for characterization to be reliably obtained.
Fig. 3B —28-year-old woman with renal angiomyolipoma.
B, Follow-up renal MR image shows lesion (arrow) with hyperintensity on in-phase unenhanced T1-weighted 2D spoiled gradient-echo sequence.
Fig. 3C —28-year-old woman with renal angiomyolipoma.
C, Follow-up renal MR image shows that lesion (arrow) remains hyperintense on out-of-phase sequence and has signal loss at its interface with normal adjacent parenchyma (India-ink artifact), consistent with fat.

Results

Subjects

The study group comprised patients (28 men, 27 women; mean age, 44 years; age range, 20–69 years) who had one or more small renal lesion (< 15 mm) that was seen on screening CT and then was further evaluated using MRI. The mean interval between the CT and MRI examinations was 40 days (range, 1–105 days). All CT and MRI examinations were deemed adequate for image interpretation. The two reviewers were in complete agreement regarding characterization of each lesion by CT and MRI.

Lesions Detected by CT

The 55 patients in our study had a total of 105 incidental lesions identified by CT. Eleven of these 105 lesions could be characterized by CT, including four lesions that were 15 mm or larger (one Bosniak IIF renal cystic lesion, one Bosniak III renal cystic lesion, one simple cyst, and one proteinaceous or hemorrhagic cyst) and seven lesions that were smaller than 15 mm (three simple cysts, two angiomyolipomas, one Bosniak II renal cystic lesion, and one solid renal mass). Thus, for our cohort of 55 patients, 94 lesions, all of which were less than 15 mm in diameter, remained incompletely characterized by CT. Of these 94 lesions, 18 were 0–3 mm, 49 were 4–6 mm, 21 were 7–9 mm, five were 10–12 mm, and one was 14 mm in diameter.

Lesion Characterization by MRI

Of the 94 small lesions that were incompletely characterized by CT, 93 (99%) were confidently characterized by MRI; 83 of these lesions were simple cysts, eight were proteinaceous or hemorrhagic cysts, and two were angiomyolipomas. A single lesion had low signal on both T1- and T2-weighted images did not show signal drop-out on opposed-phase imaging or definite enhancement on contrast-enhanced images, although evaluation was somewhat limited given the presence of a minor respiratory misregistration artifact on subtraction images. This lesion remained categorized as an indeterminate lesion after MRI examination.

Outcomes

Of the 55 patients who underwent MRI, 45 (82%) eventually donated a kidney. Of the remaining 10 patients, one did not proceed to donation owing to a renal lesion. This patient had a 10-mm solid enhancing renal mass, the appearance of which was subtle on CT because of its polar location, small size, and near isoenhancement to the parenchyma on contrast-enhanced phase images. This mass was not seen prospectively by the radiologist but was discovered on subsequent MRI examination, which had been performed to evaluate an indeterminate lesion present in the other kidney (Fig. 4). Both patients who had angiomyolipomas characterized only by MRI donated their kidneys. In both cases, the choice was made by the transplant surgeon to recover the kidneys containing the angiomyolipomas. For the patient with the single renal lesion that was indeterminate by both CT and MRI, the choice was made to donate the kidney with the single lesion. No notation was made in the operative note of a solid lesion in this kidney during its back-bench preparation. Therefore, in our cohort, MRI directed the management of four patients (7%). None of the renal donor patients had follow-up imaging of their lesions performed at our institution.
Fig. 4A —65-year-old woman with solid renal mass.
A, Axial CT nephrographic phase image shows subtle enhancing 10-mm mass (arrow) on anterior aspect of superior right kidney that was not prospectively identified on CT. Lesion (arrowhead) considered too small to characterize is seen posterior to this mass.
Fig. 4B —65-year-old woman with solid renal mass.
B, Mass (arrow) readily identified on MR image shows intermediate hyperintensity on axial fat-saturated T2-weighted sequence. Lesion (arrowhead) considered too small to characterize represents tiny simple cyst with T2 hyperintensity.
Fig. 4C —65-year-old woman with solid renal mass.
C, Mass (arrow) readily identified on MR image shows enhancement on axial contrast-enhanced subtracted T1-weighted sequence. Lesion (arrowhead) considered too small to characterize represents tiny simple cyst without enhancement.

Discussion

Preoperative imaging of potential kidney donors is necessary before kidney procurement. Patients who have a complex cystic or solid renal mass, including angiomyolipomas, diagnosed by preoperative imaging may be deemed ineligible to be kidney donors, or they may be directed to donate the affected kidney and may sometimes require ex vivo assessment and resection of the mass. Small renal lesions (< 15 mm) often cannot be fully characterized by CT examination. At our institution, therefore, renal lesions of indeterminate classification that are seen on screening CT examination of renal donor patients are further evaluated by MRI. Of the 94 small indeterminate lesions seen on CT performed for this cohort of patients, 93 (99%) could be confidently characterized by MRI, and all 93 of these ended up being characterized as benign lesions.
Our study shows that small renal lesions that are classified by CT as being too small to characterize can be characterized noninvasively by MRI. In addition, we found that nearly all of the lesions in our study were benign, although two were small angiomyolipomas. MRI findings allowed a confident decision to be made by the transplant surgeons with respect to removing the kidney affected by angiomyolipoma from these potential donors. The single lesion that remained categorized as an indeterminate lesion after MRI examination did not show enhancement on contrast-enhanced images and may have represented a hemorrhagic cyst with chronic blood products that rendered it hypointense on both T1- and T2-weighted images.
Two main reasons account for the inability of CT to determine the nature of a small renal lesion: partial volume averaging and pseudoenhancement [5]. When the slice thickness is more than half the diameter of the lesion, volume averaging becomes more pronounced, often resulting in categorization of lesions less than 5 mm as indeterminate [13]. Partial volume averaging can be mitigated by using thin CT slices to assess the density of a lesion, but thin slices have much higher image noise, and this fact, coupled with the inherently smaller size of the circular ROI that is placed to measure the CT attenuation of these lesions, can potentially result in an erroneously higher CT number. It has been shown that CT examination of renal lesions can erroneously reveal enhancement of up to 50 HU, termed “pseudoenhancement,” which can lead to mischaracterization of a cyst as an enhancing renal mass [14]. The degree of pseudoenhancement is inversely related to the size of the renal lesions [14, 15]. This is thought to be the result of the reconstruction algorithm used in helical CT to adjust for beam caused by hardening effects [5]. MRI offers superior soft-tissue contrast when compared with CT, especially with respect to discriminating among fat, fluid, and other unenhanced soft tissues. Cystic lesions such as simple renal cysts show marked hyperintensity on T2-weighted images, and lesions with intralesional hemorrhage or high proteinaceous contents are hyperintense on T1-weighted images. Furthermore, MRI is not limited by pseudoenhancement. The use of subtraction images in MRI allows more accurate determination of the presence or absence of enhancement within renal lesions, compared with CT. Thus, MRI has the potential to characterize small lesions better than CT, as shown in our study.
Previous studies comparing MRI and CT have mostly studied larger renal lesions and have shown similar classification of lesions, regardless of the modality used [8, 16, 17]. There is some variance in the definition of diameter thresholds for characterization of indeterminate lesions [1820]. In our cohort, however, our use of a threshold of 15 mm was justified because all indeterminate renal lesions were less than 15 mm in diameter. A recent study investigated the role of MRI in characterizing indeterminate small renal masses (< 2 cm) detected on ultrasound or CT [18]. Although dedicated renal CT examinations for the purpose of characterization were only performed for approximately 25% of the lesions in that study, the mean lesion size noted was 13 mm (compared with 6 mm in our study); therefore, the results of that study support the superiority of MRI in the characterization of small renal lesions less than 2 cm in diameter. The results of our study also support MRI as offering better characterization of indeterminate small (< 15 mm) lesions seen on CT. Furthermore, the multiparametric evaluation offered by MRI allows higher confidence in diagnosing angiomyolipomas.
In the nondonor patient population, use of MRI as a follow-up examination for every incidental subcentimeter renal lesion seen on CT is not an appropriate use of resources; however, use of MRI for this purpose in the renal donor population is valid. Even though MRI classified almost all such lesions in our study as benign, the identification of a solid renal lesion or an angiomyolipoma has important surgical consequences for potential renal donors. This was exemplified by our patient who had a subcentimeter solid renal mass that was missed by CT but detected by MRI, thereby resulting in the kidney being excluded from donation. Knowledge that one of the potential donor kidneys has an angiomyolipoma may influence the transplant surgeon to use the affected kidney for donation, thereby leaving the donor with the kidney without abnormal findings. Foreknowledge that such lesions are angiomyolipomas could therefore affect the management of such donated kidneys [21]. In our study, we identified two lesions that were categorized as indeterminate lesions by CT but were designated angiomyolipomas by MRI, a reclassification that directed surgical management in both cases. Given the organ shortage, some authors have proposed the use of donor kidneys from patients with renal tumors less than 3 cm; these tumors are excised during backbench preparation of the graft [22, 23]. Excision of such tumors, including angiomyolipomas, does not seem to affect graft or recipient survival [24, 25]. The exact size thresholds delineating when to excise angiomyolipomas are unclear, although angiomyolipomas larger than 5 mm may warrant surgical excision [26]. At our institution, angiomyolipomas, regardless of their size, direct the transplant surgeon toward using the affected kidney for donation.
Our study has some limitations. First, this was a retrospective study. Second, MRI characterization of lesions was done using established criteria, and there was no follow-up pathologic examination for the renal lesions that were discovered. However, the criteria used for MRI characterization of these lesions are fairly well established. Follow-up studies confirming benignity would have been useful; however, such studies were not performed for our patients because they were otherwise healthy. The findings from follow-up studies likely would not have changed our designation of the lesions as benign, because previous studies have shown that small lesions that are characterized as benign maintain their classification on subsequent imaging [18]. Follow-up of the donated kidneys may have been helpful, but this information is difficult to procure, both because donation may occur at a different institution and because follow-up is not ensured. In addition, the natural history of the lesions in a donated kidney from a patient who is receiving immunosuppression therapy is unclear. Furthermore, other modalities, such as conventional ultrasound, contrast-enhanced ultrasound, and dual-energy CT, may prove useful in the confident categorization of small renal lesions. These modalities were not available for use in the examination of our study cohort. Future studies investigating the use of such modalities for the characterization of indeterminate small renal lesions may be helpful in lowering the cost associated with MRI examinations [2729]. Finally, our patient population was limited to a highly selected population of healthy potential renal donors and does not include the general population.
In conclusion, this study shows that, in potential renal donor patients, MRI can effectively characterize lesions that are deemed by CT to be too small to characterize, and it also can potentially alter surgical management and donor status.

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 325 - 330
PubMed: 26204282

History

Submitted: October 20, 2014
Accepted: December 3, 2014

Keywords

  1. indeterminate renal lesions
  2. renal mass
  3. renal transplant
  4. small renal lesions
  5. too small to characterize

Authors

Affiliations

Ghaneh Fananapazir
Department of Radiology, University of California Davis Medical Center, 4860 Y St, Ste 3100, Sacramento, CA 95817.
Ramit Lamba
Department of Radiology, University of California Davis Medical Center, 4860 Y St, Ste 3100, Sacramento, CA 95817.
Brittany Lewis
University of California Davis Medical Center, Sacramento, CA.
Michael T. Corwin
Department of Radiology, University of California Davis Medical Center, 4860 Y St, Ste 3100, Sacramento, CA 95817.
Sima Naderi
Department of Radiology, University of California Davis Medical Center, 4860 Y St, Ste 3100, Sacramento, CA 95817.
Christoph Troppmann
Department of Surgery, University of California Davis Medical Center, Sacramento, CA

Notes

Address correspondence to G. Fananapazir ([email protected]).

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