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Complex Posttransplantation Abnormalities of Renal Allografts: Evaluation with MR Imaging¹

¹ From the Departments of Radiology (M.G.A., F.V.C., H.H.) and Surgery (P.N.B.), University of California, 505 Parnassus Ave, San Francisco, CA 94143. From the 1997 RSNA scientific assembly. Received January 15, 1998; revision requested March 23; final revision received August 5; accepted November 6. Address reprint requests to F.V.C.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To assess the efficacy of magnetic resonance (MR) imaging in the evaluation of complex abnormalities of renal allografts.

MATERIALS AND METHODS: Clinical and radiologic findings were retrospectively reviewed in 24 patients who underwent MR imaging of a renal allograft because ultrasonographic (US) findings were inconclusive or discordant with clinical findings. The final diagnoses were established with histopathologic analysis (n = 16) or clinical and imaging follow-up (n = 8).

RESULTS: MR imaging diagnoses were correct in 16 patients (67%), whereas US diagnoses were correct in six patients (25%) (P < .05). Five cases of allograft involvement by posttransplantation lymphoproliferative disorder (PTLD) were found at histopathologic analysis; at MR imaging, PTLD appeared as hypointense masses on T1- and T2-weighted images with minimal enhancement. In four of the five cases of PTLD, the masses occurred at the renal hilum and encased hilar vessels. Normal morphology was correctly diagnosed with MR imaging in five patients in whom a mass was suspected at US.

CONCLUSION: MR imaging results are often diagnostic in cases of complex abnormalities of renal allografts. Renal allograft involvement by PTLD appears to have a relatively characteristic MR imaging appearance. Normal MR imaging findings in cases of suspected masses at US may obviate biopsy.

Index terms: Grafts, 81.455 • Kidney, MR, 81.1214, 81.12143 • Kidney, transplantation, 81.455 • Kidney, US, 81.1298, 81.12983

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Renal transplantation is the preferred mode of renal replacement therapy in end-stage renal disease because both long-term survival and quality of life are improved when transplantation is performed instead of hemodialysis (1,2). Transplantation is also more cost-effective than hemodialysis (2). Complications of transplantation include peritransplant fluid collections, vascular and urologic complications, infection, rejection, malignancy, reactions to nephrotoxic drugs, and recurrent disease (3–5). Gray-scale ultrasonography (US) is the primary modality for imaging these complications, which may manifest as parenchymal or peritransplant abnormalities or as pelvicaliectasia (6). In addition, duplex and color Doppler US may help detect vascular complications. However, on occasion US findings may be nonspecific. For example, focal or diffuse alterations in the parenchymal echogenicity of renal allografts may represent rejection, malignancy, infection, or infarction. Because the findings are nonspecific, percutaneous biopsy may be required. Complications of biopsy of renal allografts include hemorrhage, pseudoaneurysm, arteriovenous fistula, and laceration of the collecting system (6). Therefore, noninvasive methods for further evaluation are desirable.

Magnetic resonance (MR) is an excellent modality for renal imaging, although US and computed tomography (CT) remain the primary modalities for cost reasons (7). The principal current applications of renal MR imaging are in patients with renal failure or complex lesions and in patients who have had a clinically important reaction to intravenously administered iodinated contrast medium. The role of MR imaging in renal allograft disease is not clearly established (1), but MR imaging remains an attractive modality when compared with US or CT because of superior contrast resolution, multiplanar capability, lack of operator dependence, and no need for intravenous iodinated contrast medium. Also, MR imaging has the general potential for increased characterization of abnormalities detected with US or CT; this potential for increased characterization has been shown to have a substantial effect on clinical management in hepatic and gynecologic imaging (8,9).

We undertook a study to assess the efficacy of MR imaging in the evaluation of posttransplantation renal allograft abnormalities when US findings are inconclusive or discordant with clinical findings.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
Between June 1989 and June 1997, 1,992 renal transplantations were performed at our institution. A retrospective review was performed to identify all renal allograft recipients who underwent MR imaging of the allograft during this period. Inclusion criteria were as follows: (a) MR imaging performed for further evaluation of an abnormality seen or suspected at US or for discordance between clinical and US findings, (b) MR imaging performed within 7 days of US or within 30 days in cases of suspected renal allograft masses at US, and (c) availability of a standard of reference for final diagnosis.

Twenty-four of 40 patients who underwent MR imaging of the renal allograft during the study period met all of the inclusion criteria. The total number of renal transplants studied was 27 because one patient had received three renal allografts, two of which were chronically rejected, and another patient had undergone en bloc transplantation of both kidneys from a pediatric donor (10). There were 14 male and 10 female patients with a mean age of 48 years (range, 15–62 years). The interval since transplantation was 3 months or less in six patients and more than 3 months in the remainder. Indications for US were impaired renal function (n = 18), fever (n = 2), and trauma (n = 1). No reason was given in three cases.

The US findings and the reasons for requesting MR imaging were as follows:

1. US demonstrated a definite or possible mass in 11 patients. MR imaging was requested for further assessment.

2. US demonstrated a morphologic abnormality suggestive of rejection in four patients. Abnormalities considered suggestive of rejection at our institution include loss of corticomedullary differentiation, pyramidal swelling, increased parenchymal echogenicity, pelviinfundibular wall thickening, and renal swelling. In three patients, MR imaging was requested because of clinical findings suggestive of sepsis. In the fourth patient, MR imaging was performed as part of a separate study of MR imaging in renal allograft rejection.

3. US demonstrated a nonspecific peritransplant fluid collection in three patients. All three patients had declining renal function. MR imaging was requested because a suspected hematoma at US was not resolving on serial studies (n = 1), because it was unclear whether the fluid collection was separate from adjacent ascites (n = 1), and because of coexistent fever (n = 1).

4. US demonstrated possible renal vein thrombosis in two patients. MR imaging was requested because of lack of certainty about the US diagnosis.

5. US demonstrated a raised resistive index without clinically important abnormal morphology in two patients. MR imaging was requested because of declining renal function that was not adequately explained by the US findings.

6. US demonstrated wedge-shaped hypoechoic lesions suggestive of infarction in one patient. MR imaging was requested because of lack of certainty about the US diagnosis.

7. US demonstrated normal morphology in one patient. MR imaging was requested because of declining renal function that was not explained by the US findings.

The mean interval between US and MR imaging was 2.5 days (range, 0–30 days). Final diagnoses were established with histopathologic correlation (n = 16) or clinical and imaging follow-up (n = 8). Histopathologic specimens were obtained by means of percutaneous biopsy or aspiration (n = 12) or transplant nephrectomy (n = 4). Diagnoses established with histopathologic correlation were rejection (n = 5), posttransplantation lymphoproliferative disorder (PTLD) (n = 5), infection (n = 3), lymphocele (n = 1), toxic reaction to cyclosporine (n = 1), and normal morphology (n = 1). Diagnoses established with clinical and imaging follow-up were normal morphology (n = 5; minimum follow-up of 1 year), renal vein thrombosis (n = 1; confirmed with conventional angiography), angiomyolipoma (n = 1; follow-up of 2 years), and ascites (n = 1; confirmed with serial US subsequent to MR imaging).

Imaging Technique
US was performed with state-of-the-art equipment, 3.5–5.0-MHz transducers, and a combined gray-scale and color Doppler technique. All US scans were reviewed and reported by attending radiologists with extensive experience in US. MR imaging was performed with a 1.5-T unit (Signa; GE Medical Systems, Milwaukee, Wis) and phased-array surface coils. T1-weighted spin-echo images (repetition time msec/echo time msec = 600–700/11–17) and T2-weighted conventional (2,000/80–100) or fast (3,000–5,000/85–120) spin-echo images were acquired in all patients. Intravenous gadolinium contrast medium (0.1 mmol/kg) was administered in 23 of the 24 patients. Gadolinium-enhanced T1-weighted spin-echo images were acquired with the same parameters as the nonenhanced T1-weighted images. The MR imaging findings were reported by attending radiologists experienced in MR imaging who had a special interest in genitourinary radiology. Clinical and prior imaging results were available to the radiologists who reported the MR imaging findings.

Analysis of MR Imaging Findings
The efficacy of MR imaging was established by reviewing the original MR imaging reports. The original impression was compared with the established final diagnosis and categorized as correct (if the leading diagnosis in the report was the final diagnosis) or incorrect (if the leading diagnosis in the report was not the final diagnosis). If the original impression was concordant with the final diagnosis but the report did not specifically give the final diagnosis as the leading diagnosis, the original impression was considered incorrect. The same categorization was performed for the original US reports. The performance of US and that of MR imaging were compared by means of the McNemar test with the Yates correction. In cases of PTLD, the signal intensity and enhancement characteristics were determined with consensus review of the images by three radiologists (M.G.A., F.V.C., H.H.) because, in some cases, these features were incompletely described in the original report. However, the leading diagnosis given in the original report was never altered and remained the sole basis for the analysis of efficacy.

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The final diagnoses are shown in Table 1. The US and MR imaging results are shown in Table 2. There were five cases of renal allograft involvement by PTLD, which manifested as hypointense masses on T1- and T2-weighted images with minimal enhancement on postcontrast images (Figs 1–3). In four of the five cases, PTLD manifested as a peritransplant mass at the renal hilum that encased traversing hilar vessels. In the fifth case, which occurred in a patient with three renal allografts, PTLD manifested as multiple solid masses in the parenchyma of two of the allografts. The third allograft was too atrophic to determine if intrarenal masses were present.

View larger version (186K): [in this window] [in a new window]   Figure 1a. Patient 18. Impaired renal function due to PTLD involving the hilum of the allograft in a 55-year-old man 8 months after renal transplantation. (a) Transverse US scan shows a nonspecific, ill-defined, hypoechoic mass (arrows) at the hilum of the allograft. (b) Axial fast spin-echo T2-weighted MR image (5,000/85) shows an inhomogeneous mass (arrows) at the hilum of the allograft. The mass is hypointense to the renal parenchyma, a finding suggestive of PTLD.

View larger version (154K): [in this window] [in a new window]   Figure 1b. Patient 18. Impaired renal function due to PTLD involving the hilum of the allograft in a 55-year-old man 8 months after renal transplantation. (a) Transverse US scan shows a nonspecific, ill-defined, hypoechoic mass (arrows) at the hilum of the allograft. (b) Axial fast spin-echo T2-weighted MR image (5,000/85) shows an inhomogeneous mass (arrows) at the hilum of the allograft. The mass is hypointense to the renal parenchyma, a finding suggestive of PTLD.

View larger version (139K): [in this window] [in a new window]   Figure 2a. Patient 13. PTLD involving the hilum of the allograft in a 19-year-old man 6 months after renal transplantation. The results of US-guided fine-needle aspiration biopsy were inconclusive; the PTLD was discovered at follow-up US. (a) Axial spin-echo T1-weighted MR image (700/17) shows an ill-defined mass (*) at the hilum of the allograft. The mass is slightly hypointense to the renal parenchyma. Blood in the dependent portions of the renal calices (arrows) is due to hemorrhage from prior biopsy. (b) Gadolinium-enhanced axial spin-echo T1-weighted MR image (700/17) shows only mild enhancement of the mass.

View larger version (136K): [in this window] [in a new window]   Figure 2b. Patient 13. PTLD involving the hilum of the allograft in a 19-year-old man 6 months after renal transplantation. The results of US-guided fine-needle aspiration biopsy were inconclusive; the PTLD was discovered at follow-up US. (a) Axial spin-echo T1-weighted MR image (700/17) shows an ill-defined mass (*) at the hilum of the allograft. The mass is slightly hypointense to the renal parenchyma. Blood in the dependent portions of the renal calices (arrows) is due to hemorrhage from prior biopsy. (b) Gadolinium-enhanced axial spin-echo T1-weighted MR image (700/17) shows only mild enhancement of the mass.

View larger version (163K): [in this window] [in a new window]   Figure 3a. Patient 5. Impaired renal function due to PTLD involving the renal allografts in a 53-year-old woman 5 months after en bloc transplantation of both kidneys from a pediatric donor. (a) Oblique sagittal US image shows an ill-defined, hypoechoic lesion (black arrows) between the two allografts (white arrows). (b) Sagittal fast spin-echo T2-weighted MR image (3,000/102) of the right iliac fossa shows a hypointense mass (black arrows) between the allografts (white arrows). The mass extends into both renal hila.

View larger version (155K): [in this window] [in a new window]   Figure 3b. Patient 5. Impaired renal function due to PTLD involving the renal allografts in a 53-year-old woman 5 months after en bloc transplantation of both kidneys from a pediatric donor. (a) Oblique sagittal US image shows an ill-defined, hypoechoic lesion (black arrows) between the two allografts (white arrows). (b) Sagittal fast spin-echo T2-weighted MR image (3,000/102) of the right iliac fossa shows a hypointense mass (black arrows) between the allografts (white arrows). The mass extends into both renal hila.

Five of 11 patients with a US diagnosis of a mass or a possible mass in the allograft had normal MR images. In these five patients, there was normal parenchymal signal intensity with all sequences and normal uniform enhancement on postcontrast images. All five patients had normal serial follow-up images, and the final diagnosis was normal morphology in all five (Fig 4).

View larger version (159K): [in this window] [in a new window]   Figure 4a. Patient 6. Morphologically normal allograft in a 41-year-old man with a history of recent trauma 13 years after renal transplantation. The final diagnosis was based on results of serial follow-up imaging. (a) Transverse US scan of the renal allograft shows a possible hypoechoic mass (arrows). (b) Gadolinium-enhanced axial spin-echo T1-weighted MR image (500/8) shows normal enhancement of a prominent hilar lip (arrows) with no evidence of a mass.

View larger version (145K): [in this window] [in a new window]   Figure 4b. Patient 6. Morphologically normal allograft in a 41-year-old man with a history of recent trauma 13 years after renal transplantation. The final diagnosis was based on results of serial follow-up imaging. (a) Transverse US scan of the renal allograft shows a possible hypoechoic mass (arrows). (b) Gadolinium-enhanced axial spin-echo T1-weighted MR image (500/8) shows normal enhancement of a prominent hilar lip (arrows) with no evidence of a mass.

View larger version (147K): [in this window] [in a new window]   Figure 5. Patient 15. Fever and US findings suggestive of rejection in a 25-year-old woman 2 months after renal transplantation. Axial spin-echo T1-weighted MR image (500/17) of the left iliac fossa shows a normal allograft (*) with no loss of corticomedullary differentiation or other changes suggestive of rejection. A fine-needle aspiration biopsy specimen demonstrated rejection.

View larger version (180K): [in this window] [in a new window]   Figure 6a. Patient 10. Impaired renal function in a 38-year-old man 1 year after renal transplantation. (a) Oblique sagittal US scan shows a 4.3-cm-diameter hypoechoic lesion (*) at the hilum of the allograft. This finding was interpreted as a solid mass. Measurement cursors are included on the image. (b) Axial fast spin-echo T2-weighted MR image (4,000/105) of the left iliac fossa shows a hyperintense lesion (*) adjacent to the allograft (arrow), a finding consistent with a fluid collection. A lymphocele was confirmed with CT-guided aspiration.

View larger version (157K): [in this window] [in a new window]   Figure 6b. Patient 10. Impaired renal function in a 38-year-old man 1 year after renal transplantation. (a) Oblique sagittal US scan shows a 4.3-cm-diameter hypoechoic lesion (*) at the hilum of the allograft. This finding was interpreted as a solid mass. Measurement cursors are included on the image. (b) Axial fast spin-echo T2-weighted MR image (4,000/105) of the left iliac fossa shows a hyperintense lesion (*) adjacent to the allograft (arrow), a finding consistent with a fluid collection. A lymphocele was confirmed with CT-guided aspiration.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

Immunosuppression causes a hundredfold increase in the prevalence of cancer in transplant recipients compared with the prevalence in the age-matched general population (11). Non-Hodgkin lymphoma and squamous cell carcinoma of the skin and lips are the most common posttransplantation cancers. PTLD is a potentially fatal, lymphomalike lymphoid proliferation that is associated with Epstein-Barr virus and occurs in approximately 2% of solid-organ transplant recipients (12). PTLD was reported after the introduction of cyclosporine as the principal immunosuppressive agent for transplant recipients (13,14). PTLD differs from classic non-Hodgkin lymphoma in that the proliferating lymphocytes are more polymorphic and may be polyclonal rather than monoclonal. Also, PTLD may regress with reduction or cessation of cyclosporine therapy and may not respond to conventional antilymphoma chemotherapy.

Common sites of involvement by posttransplantation lymphoma and PTLD are the brain, lymph nodes, gastrointestinal tract, and lungs (14–16). The renal allograft is an inconstantly described site of involvement. No transplant involvement was found in five renal allograft recipients with cyclosporine-induced PTLD (14). Four renal allografts were involved in 15 patients with posttransplantation lymphoma; two of these renal allografts demonstrated centrally hypoattenuating masses adjacent to the kidney at CT and two demonstrated no radiologic abnormalities (15). Three of six renal allograft recipients with posttransplantation abdominal lymphoma demonstrated poorly defined masses infiltrating the allograft at CT (16).

The MR imaging findings in renal allograft involvement by PTLD have not been described, to our knowledge. We found a relatively typical pattern: a hilar mass that was hypointense on T1- and T2-weighted images, contained traversing renal vessels, and demonstrated minimal enhancement. This pattern was seen in four of the five cases. One case demonstrated multiple solid lesions in the allograft parenchyma; the correct diagnosis was suggested by the signal intensity characteristics. All but one of the five cases were correctly diagnosed with MR imaging; the false-negative diagnosis was due to mischaracterization of a hilar mass as a possible hematoma. This case occurred in the 1st year of the study and was considered suggestive of PTLD when reviewed in the context of our subsequent experience.

The predilection of renal allograft PTLD for the renal hilum is noteworthy. The hepatic hilum was the site of hepatic transplant involvement by PTLD in three of three cases (17); it is possible that the perianastomotic region of a solid-organ transplant is somehow predisposed to the development of PTLD. Diagnosis of allograft involvement by PTLD by means of fine-needle aspiration biopsy may be difficult because the predilection of PTLD to encase the hilar vessels increases the risk of hemorrhage and because the cytologic diagnosis is not straightforward (12). Therefore, recognition of the MR imaging features of PTLD may be helpful in the diagnostic evaluation of peritransplant masses.

US has recognized limitations in the detection of small renal lesions (18). These limitations may result in a lowered threshold for reporting possible masses, especially in patients with an increased risk of malignancy, such as transplant recipients. Our results suggest that MR imaging may be helpful in establishing the normality of suspected masses at US and thus obviate biopsy. In our study, all five cases of normal morphology with a false-positive US diagnosis of a mass had unremarkable clinical and serial follow-up imaging findings.

There are three potential criticisms of our study. First, the study population was relatively small despite an 8-year study period. The smallness of the study population likely reflects the adequacy of clinical and US evaluation, supplemented by biopsy as necessary, in the majority of posttransplantation renal allograft abnormalities. In addition, the smallness of the study population may reflect lack of awareness of the potential of MR imaging and financial constraints on high-technology imaging. Second, the study was performed retrospectively and was based on the original MR imaging reports, which were generated by radiologists with knowledge of the clinical results and other radiologic results. Their knowledge of these additional results explains why some of the leading diagnoses in Table 2 may not intuitively appear to follow directly from the described imaging findings. For example, the small intrarenal fluid collections seen at MR imaging in patient 7 were considered likely to be abscesses rather than cysts because the history of fever was available. Basing the study on the original MR imaging reports may have introduced bias but has the advantage of producing results that represent the real-life incremental benefit of MR imaging, and one of our aims was to investigate the clinical role of MR imaging in this patient population. Third, there was a definite selection bias in our study population because only patients with US findings that were inconclusive or discordant with clinical findings were included. Nonetheless, we specifically wished to evaluate patients with complex lesions that were indeterminate at US. We are not suggesting that MR imaging should be used routinely in the evaluation of renal allograft abnormalities.

In conclusion, MR imaging often provides specific diagnostic information in cases of complex posttransplantation abnormalities of renal allografts. Renal allograft involvement by PTLD appears to have a relatively characteristic MR imaging appearance. Normal MR imaging findings in cases of suspected masses at US may obviate biopsy.

	Footnotes

 
Abbreviation: PTLD = posttransplantation lymphoproliferative disorder

Author contributions: Guarantor of integrity of entire study, H.H.; study concepts, H.H.; study design, M.G.A., F.V.C.; definition of intellectual content, H.H., F.V.C.; literature research, M.G.A., F.V.C.; data acquisition and analysis, M.G.A., F.V.C.; statistical analysis, H.H., F.V.C.; manuscript preparation, F.V.C.; manuscript editing, H.H., F.V.C.; manuscript review, P.N.B.

	References

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ali, M. G. Articles by Bretan, P. N. Search for Related Content PubMed PubMed Citation Articles by Ali, M. G. Articles by Bretan, P. N.