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Renal Transplant Imaging Using Magnetic Resonance Angiography With a Nonnephrotoxic Contrast Agent

Bashir, Mustafa R.1,5; Jaffe, Tracy A.1; Brennan, Todd V.2; Patel, Uptal D.3,4; Ellis, Matthew J.2,4

doi: 10.1097/TP.0b013e318295464c
Clinical and Translational Research
Free

Background In renal allograft recipients presenting with graft dysfunction, it is critical to determine the patency of the transplant vasculature to guide clinical management. Conventional modalities such as Doppler ultrasound, contrast-enhanced computed tomography, magnetic resonance angiography (MRA), and noncontrast MRA are each of limited use because of technical factors and toxicity of standard contrast agents. The purpose of this study was to retrospectively review our institutional experience with renal transplant MRA using ferumoxytol (a nonnephrotoxic medication) as a contrast agent and evaluate its use in the assessment of allograft vascular patency in patients with graft dysfunction, either delayed or slow graft function within hours to days after kidney transplantation or acute kidney injury weeks to months after kidney transplantation.

Methods Sixteen kidney transplant recipients were retrospectively identified who underwent ferumoxytol-enhanced MRA after a nondiagnostic ultrasound for kidney dysfunction after transplantation. Image evaluation was performed by two radiologists, and clinical follow-up data were collected.

Results In 1 of 16 subjects, MRA with ferumoxytol demonstrated complete arterial occlusion of an allograft. In 2 of 16 subjects, MRA detected moderate to severe anastomotic stenoses, which were confirmed at catheter angiography and successfully treated, resulting in the improvement of graft function. In 13 of 16 subjects, MRA demonstrated normal graft vasculature, and an alternative cause of allograft dysfunction was ultimately confirmed.

Conclusions Our study suggests that ferumoxytol-enhanced MRA may be a novel, safe method to accurately detect graft artery abnormalities in renal transplant recipients without the risk of nephrotoxicity, when transplant ultrasound is nondiagnostic.

1 Department of Radiology, Duke University Medical Center, Durham, NC.

2 Department of Surgery, Duke University Medical Center, Durham, NC.

3 Department of Pediatrics, Duke University Medical Center, Durham, NC.

4 Department of Medicine, Duke University Medical Center, Durham, NC.

5 Address correspondence to: Mustafa R. Bashir, M.D., Department of Radiology, Duke University Medical Center, 3808 Durham, NC.

The authors declare no funding or conflicts of interest.

E-mail: mustafa.bashir@duke.edu

M. R. B. and M. J. E. participated in making the research design, performing the research, analyzing the data, and writing the paper. T. A. J. participated in performing the research, analyzing the data, and writing the paper. T. V. B. and U. D. P. participated in analyzing the data and writing the paper.

Received 7 March 2013. Revision requested 19 March 2013.

Accepted 2 April 2013.

Renal transplant artery stenosis often presents with posttransplantation hypertension, increase in total body fluid, and graft dysfunction. It may occur at any time after operation but usually manifests between 3 months and 2 years after transplantation. Risk factors include anastomotic stenosis related to operative techniques and atherosclerotic disease, cytomegalovirus infection, and delayed graft function (1–3). Timely assessment of renal allograft vascular patency is critical in the setting of an acute decline in graft function. Diagnosis relies on various imaging techniques but is typically performed using ultrasonography. However, this imaging modality may be limited by patient body habitus and the interposition of bowel gas between the ultrasound transducer and the allograft (4, 5). In addition, ultrasound assessment relies on waveform and flow velocity measurements, which are highly dependent on both operator and patient factors and may not accurately diagnose vascular compromise, particularly in the early postoperative period and in the presence of vessel tortuosity (4, 6).

For these reasons, an anatomic imaging technique such as computed tomography (CT) or magnetic resonance imaging (MRI) is preferred for accurate measurements of vessel patency. Unfortunately, CT and MRI using traditional contrast agents are contraindicated in the setting of impaired renal function because of the risks of contrast-induced nephropathy and nephrogenic systemic fibrosis, respectively (7–11). Ferumoxytol (Feraheme; AMAG Pharmaceuticals, Inc., Cambridge, MA) is an intravenous iron preparation consisting of carbohydrate-coated, superparamagnetic iron oxide nanoparticles used for the treatment of anemia of chronic kidney disease (CKD). It has been used in the magnetic resonance angiography (MRA) of the central nervous system and lower extremities, and it may represent an alternative to gadolinium-based agents for the vascular assessment of renal allografts (12–15). The purpose of this study is to review our initial institutional experience using ferumoxytol as a nonnephrotoxic MRA contrast agent for the assessment of kidney allograft vasculature.

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RESULTS

All 16 patients presented with acute kidney injury (AKI; n=14) weeks to months after transplantation or had slow or delayed graft function within hours to days after transplantation, manifesting as anuria/oliguria and persistently elevated creatinine levels (n=2; postoperative days 1 and 2, respectively). Of those presenting with AKI, allografts had been placed at least 5 months previously in most patients (n=12), whereas two patients presented at 12 and 17 days after operation. The original causes of renal failure necessitating transplantation in the study population included diabetic nephropathy (n=10); long-standing systemic hypertension (n=2); and hepatorenal syndrome, autosomal dominant polycystic kidney disease, focal segmental glomerulosclerosis, and chronic obstructive uropathy (each n=1).

All patients were initially evaluated by physical examination and laboratory assessment for common causes of graft dysfunction, including volume depletion, urinary obstruction, high calcineurin inhibitor trough levels, and infection. When creatinine levels remained elevated despite the correction of these etiologies, further workup with kidney transplant ultrasound was undertaken. In these 16 patients, ultrasound was either nondiagnostic or equivocal with regard to graft vessel patency, and MRA was undertaken for further assessment of vessel patency.

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Imaging

Both radiologists concluded that one graft’s arterial system was completely occluded, two transplant renal arteries were stenotic, and 13 patients’ transplant renal arteries were widely patent. In the case of arterial occlusion, the pre-MRA ultrasound was inconclusive because of artifacts from bowel overlying the allograft. MRA demonstrated complete occlusion of the transplant renal artery and the ipsilateral external iliac artery, and extensive aortoiliac atherosclerosis, and the arterial occlusion was believed to be caused by spontaneous iliac artery dissection. The graft kidney was edematous and amorphous with the absence of normal corticomedullary differentiation, and infarction was diagnosed at the time of MRA. In both cases of anastomotic stenosis, catheter angiography was undertaken and confirmed the presence of hemodynamically significant stenoses. Angioplasty was then performed in both cases, with radiographic resolution of the stenoses.

For the 15 nonoccluded grafts, mean ratings of arterial visualization on MRA ranged from 3.5 (second-order arterial branches) to 4 (iliac arteries), out of a maximum possible rating of 4. For venous segments, mean vessel visualization scores ranged from 3.6 (segmental venous branches) to 4 (iliac and main renal veins). Signal intensity ratio calculations demonstrated measurable enhancement of the graft renal cortex (1.1–1.5, P<0.01) and medulla (0.9–1.4, P<0.005) in all cases, with the exception of the occluded graft, in which there was no enhancement.

Each subject received a mean (SD) of 253 (48) mg of ferumoxytol for the MRA imaging procedure (range, 171–345 mg), which was substantially lower than the total dose routinely used for the treatment of iron-deficiency anemia at our institution (1020 mg divided for two doses). No allergic reactions or other immediate complications were observed after ferumoxytol administration.

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Clinical Outcomes With Positive MRA Examinations

Of the 16 MRA examinations, 3 demonstrated abnormal findings related to the renal graft vasculature. The case of arterial occlusion occurred in a patient with an allograft placed 11 years before the acute event (Fig. 1). This patient’s renal function deteriorated rapidly, and hemodialysis was initiated shortly after MRA demonstrated an unsalvageable, infarcted kidney. The two cases where MRA demonstrated moderate to severe anastomotic stenoses were imaged 5 and 7 months after graft placement, respectively, and presented with slowly rising creatinine levels (representative example shown in Fig. 2) or serum creatinine measurements that were above expected levels based on donor and recipient clinical variables. In both cases, catheter-based angioplasty was performed with radiographic resolution of the stenoses; stent placement was not performed in either case. Renal function improved after angioplasty, with serum creatinine levels improving from 4.4 to 2.1 mg/dL in one case, and 5.4 to 1.1 mg/dL in the other.

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

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Clinical Outcomes With Negative MRA Examinations

Of 16 MRA examinations, 13 were negative for findings related to the renal graft vasculature (representative example shown in Fig. 3). In one case, the patient had extensive contralateral iliofemoral venous thrombosis (which was observed on the MRA) and pulmonary thromboembolism, and expired later during that hospitalization from complications of pulmonary embolism. In a second case, the cause of graft dysfunction was determined to be transplant ureteral stricture with obstruction (which was demonstrated by the MRA examination), and the patient was treated with percutaneous nephrostomy. In a third case, transplant biopsy demonstrated acute on chronic rejection, and the patient eventually went on to receive a transplant nephrectomy.

FIGURE 3

FIGURE 3

In the 10 remaining cases with a negative MRA examination, an alternative cause of graft dysfunction was eventually found, including prerenal azotemia caused by other acute illnesses (pancreatitis, n=3; overdiuresis, n=2; urinary tract infection, n=2; and vomiting related to gastrointestinal illness, n=2) and postoperative hypotension from surgery not involving the transplant organ (n=1). In six of these cases, MRA was performed more than 3 months after allograft placement (and therefore, a posttransplant, pre-MRA baseline creatinine level had been established); clinical follow-up data were available over a mean (SD) of 9 (3) months (range, 6–12 months). Renal function stabilized to a mean (SD) serum creatinine level of 1.8 (0.2) mg/dL (range, 1.6–2.0 mg/dL) compared with mean (SD) baseline serum creatinine levels of 1.7 (0.1) mg/dL (range, 1.6–1.9 mg/dL) with supportive therapy/volume expansion (and antibiotics in two cases) and no direct intervention on the renal allografts. In the remaining four patients with negative MRA examinations, MRA was performed less than 3 weeks after allograft placement (on postoperative days 1, 2, 12, and 17 days, respectively), and so, a baseline posttransplantation pre-MRA creatinine was not considered to have been confidently established. All four of these patients also did well, with follow-up data available for a mean (SD) period of 5 (4) months (range, 1–9 months) and a mean (SD) serum creatinine level of 1.2 (0.2) mg/dL (range, 1.0–1.4 mg/dL) at the last follow-up.

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DISCUSSION

This study demonstrates the novel use of ferumoxytol as an intravenous contrast agent for MRA assessment of transplant vascular patency. In our small study, three significant transplant vascular abnormalities were detected, which were not definitively diagnosed by ultrasonography and could not safely or effectively be assessed with other imaging modalities. Among these, two transplant artery stenoses were detected by MRA, and catheter-based treatment resulted in the improvement in transplant function. In the case of complete arterial occlusion and transplant infarction, the allograft was definitively determined to be unsalvageable by imaging. As a result, unnecessary catheter-based evaluation and surgical exploration were avoided. In those cases where MRA did not demonstrate a vascular abnormality, other causes of graft dysfunction or AKI were identified, and the MRA examinations successfully eliminated the need for additional vascular evaluations.

In both the immediate perioperative and during long-term postoperative periods, the initial evaluation of patients presenting with acute graft dysfunction often includes noninvasive imaging to exclude urinary obstruction and vascular compromise. This is typically performed by Doppler ultrasound, although these examinations can be difficult to interpret because of patient and technologist factors (4–6). Even under the best of technical circumstances, ultrasound results are often equivocal and inadequate to guide decisions to pursue percutaneous or surgical interventions. Imaging methods using contrast agents are attractive techniques for evaluating vascular patency. However, typical contrast agents are contraindicated in the transplantation population, particularly in the setting of AKI or CKD. Specifically, iodinated contrast agents used in CT carry the risk of contrast-induced nephropathy and worsening renal function, whereas gadolinium-based agents used in MRI are associated with nephrogenic systemic fibrosis, a debilitating and sometimes fatal disease involving fibrosis of the skin, musculoskeletal system, and visceral organs (7–10, 16, 17). Although renal transplant MRA using gadolinium-based contrast agents has been described extensively, this is contraindicated in the setting of AKI (18–21). Iron-based agents are not associated with nephrogenic systemic fibrosis and appear to have few, if any, significant deleterious adverse effects, although more recently, some concerns about hypersensitivity reactions have been raised (22).

Recently, ferumoxytol, an iron-containing medication, received approval from the Food and Drug Administration for the treatment of iron deficiency in patients with CKD (11, 17). As a contrast agent, ferumoxytol causes shortening of the T1 relaxation time of its microenvironment and, at certain concentrations, appears similarly to gadolinium-based agents on many MRI pulse sequences (13, 15, 23). In addition, Sigovan et al. (24) found that ferumoxytol-enhanced MRA provided better image quality and reduced flow artifacts compared with noncontrast MRA in dialysis fistula evaluation, with a much shorter acquisition time (19 vs. 270 s). Because little free iron is present in the ferumoxytol preparation, it can be injected rapidly without causing the reactions typical of other intravenous iron preparations. Our initial experience in renal transplant MRA with ferumoxytol has demonstrated excellent depiction of the transplant vasculature, consistent with or better than other imaging modalities or direct clinical/surgical observations. Ferumoxytol-enhanced MRA allows for direct anatomic assessment for vascular stenosis/occlusion, rather than an inferred assessment based on Doppler waveform and velocity criteria, which can be particularly unreliable in the setting of vessel tortuosity and aortoiliac atherosclerotic disease. Because ferumoxytol is an iron-based agent designed specifically for use in patients with advanced CKD, its safety profile in the transplantation population is excellent, although the reported rate of serious hypersensitivity reactions is somewhat higher (0.2%) than that associated with gadolinium-based agents such as gadoteridol (0.03%) (25, 26). In addition, the amount of ferumoxytol administered for MRA is small relative to the therapeutic dose (in this study, it ranged from 17% to 34% of our routine therapeutic dose).

Because of its large molecular weight of approximately 750 kD, ferumoxytol is not filtered in the glomeruli and behaves as a blood pool contrast agent, with a long intravascular half-life of 14 to 15 hr (13, 27, 28). This property allows for extended “vascular steady state” imaging sessions when needed to ensure high-image quality, an advantage which has been demonstrated with the gadolinium-based blood pool agent gadofosveset (29). By comparison, the low-molecular weight (non–blood pool) gadolinium-based agents traditionally used in MRA are eliminated rapidly by the kidneys, with a plasma half-life of 10 to 15 min in the presence of normal renal function (30). Leakage of these non–blood pool agents into the extravascular space also prevents high-quality steady-state imaging caused by increased background signal that may obscure major vascular structures (29). Ferumoxytol appears to provide an excellent combination of high-quality steady-state MRA properties without the potentially deleterious effects of gadolinium-based agents.

In this study, MRA was performed exclusively in patients with a nondiagnostic initial ultrasound examination. These 16 patients represent a small subset of those evaluated for graft dysfunction. During this time, 101 kidney transplantations were performed, with 34 patients experiencing at least one episode of unexpected graft dysfunction during the follow-up period, necessitating at least one (but often multiple) ultrasound examinations. A total of 486 kidney transplant ultrasounds were performed during this period, for both patients with new allografts and more remote graft placement with unexpected graft dysfunction; relatively speaking, the number of cases in which MRA was performed was quite small relative to the total number of evaluations for graft dysfunction. In addition, the cost of MRA is considerably higher than that of ultrasound (∼$3600 vs. $1000), so it is currently used only as a second-line imaging when ultrasound is nondiagnostic. It is possible that MRA could be cost effective if it provided definitive guidance for management and obviated the need for additional testing/procedures, as in the case of the patient who presented with graft artery occlusion, where catheter angiography/surgical exploration was avoided. However, we were unable to assess the downstream effects on patient care costs in the context of this retrospective study.

This study has several notable strengths. First, despite being a case series, sequential enrollment minimized selection bias. In addition, differences in exposure to ferumoxytol were minimized by the use of a consistent clinical protocol across all patients that were determined a priori between our multidisciplinary transplantation team, including members from medicine, surgery, and radiology. To our knowledge, it is the first case series describing the use of ferumoxytol-enhanced MRA for kidney transplant evaluation. It demonstrates the use of the technique in a high-risk population with no clear alternatives that are low risk or effective. Despite these strengths, however, this study also has several limitations. First, it was a single-center retrospective review with a relatively small number of cases. Second, the dose and injection protocol for ferumoxytol have not been thoroughly optimized, and anecdotally, it may be possible to obtain imaging of similar quality with a lower dose of ferumoxytol. Third, catheter-based angiography, the reference standard for luminal stenosis, was only available in a few cases, and we were forced to rely on clinical follow-up data to exclude functionally significant stenosis in most subjects. However, the study does suggest that MRA with ferumoxytol can accurately detect renal transplant artery abnormalities, and the consistently high image quality across subjects suggests that it may be more robust than conventional Doppler ultrasound evaluation.

In conclusion, based on our initial experience, renal transplant MRA with ferumoxytol is a useful diagnostic test for evaluating transplant vessel patency in the setting of allograft dysfunction. It may be a useful adjunct test when ultrasound evaluation is nondiagnostic or equivocal, and represents a novel method for anatomic depiction of allograft vascular patency without the risks associated with conventional imaging contrast agents.

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MATERIALS AND METHODS

The institutional review board approved this Health Insurance Portability and Accountability Act–compliant study and waived the requirement for informed consent because of its retrospective design.

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Study Population

The study population consisted of 16 consecutive patients with renal allografts who were imaged with MRA using ferumoxytol between October 1, 2011, and November 1, 2012. These included nine men and seven women, with a mean (SD) age of 54.4 (11.7) years (range, 36–73 years). Patients were imaged for unexpected kidney dysfunction, presenting as slow or delayed graft function immediately after allograft placement or AKI more than 1 week after transplantation. AKI was defined as an increase in the baseline creatinine of 30% or more above the nadir creatinine (the lowest measured creatinine on two or more consecutive occasions). All patients had ultrasound examinations before MRA, which were equivocal or nondiagnostic with regard to graft vessel patency.

Historical data relating to the patients’ original cause for renal transplantation, the perioperative and postoperative course of events, and the acute episode that led to the need for allograft vascular evaluation were collected.

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Imaging and Statistical Analysis

All patients underwent MRA focused on their renal allograft on either 1.5- or 3-T clinical MRI systems. First, precontrast T1- and T2-weighted imaging was performed for morphologic assessment. Then, dynamic post–contrast imaging was performed using a time-resolved pulse sequence with a 3- to 4-s frame rate, during the intravenous bolus injection of 3 mg/kg of ferumoxytol diluted with normal saline to a total bolus volume of 30 mL through a peripheral intravenous angiocatheter. Finally, contrast-enhanced anatomic imaging was performed with high-resolution T1-weighted sequence covering the renal allograft and ipsilateral iliac vessels. When available, confirmatory catheter angiography images and transplant ultrasound examinations were also reviewed. The dose of ferumoxytol administered to subjects for their MRA was also collected.

Two fellowship-trained faculty abdominal radiologists independently assessed vascular patency based on contrast-enhanced images. They rated vessel visualization on a scale of 1 (vessels not seen) to 4 (excellent visualization). Vascular segments evaluated included the iliac artery, main renal artery, segmental renal arteries, second-order arterial branches, iliac vein, main renal vein, and segmental renal veins. Signal intensity ratios normalized to muscle from the MRI examinations were measured in the graft cortex and medulla as a semiquantitative measure of small parenchymal vessel enhancement. Normalized signal intensity ratios measured before and after ferumoxytol administration were compared using a paired Student t test, with a value of P<0.05 considered statistically significant.

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Clinical Reference Standard

All available clinical follow-up data available at the time of medical record review were collected. For those patients in whom baseline posttransplantation creatinine levels were available (creatinine levels obtained >3 months after transplantation, but before MRA and not during a clinically reported episode of AKI), baseline creatinine levels were recorded. The most recent available creatinine levels were also recorded as a follow-up measure of graft function. Graft biopsy results and surgical reports were also reviewed.

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Keywords:

Kidney transplant; Magnetic resonance angiography; MRA; Ferumoxytol; Feraheme

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