- Email: [email protected]
Endovascular management of transplant renal artery stenosis
Endovascular management of transplant renal artery stenosis Joseph Touma, MD, Alessandro Costanzo, MD, Benoît Boura, MD, Faris Alomran, MD, and Myriam Combes, MD, Paris, France Objective: Most clinicians regard angioplasty with or without stent placement to be the treatment of choice for transplant renal artery stenosis (TRAS). However, published results regarding its effectiveness are heterogeneous. The aim of this study was to assess the safety and efficiency of TRAS endovascular therapy. Methods: All cases of TRAS admitted for treatment in our unit from January 2009 to December 2012 were reviewed retrospectively. The primary end point was the stenosis-free primary transplant renal artery patency. Secondary end points were freedom from reintervention, graft survival, postoperative serum creatinine level, blood pressure evolution, and the number of antihypertensive drugs pre- and postprocedure. Results: A total of 17 patients (10 men, 7 women) presenting with TRAS were referred to our institution. During the early post-transplantation process (<15 days), 35.2% of patients presented. The median time to presentation was 40 days. The predominant presentation was graft function alteration (82.3%). Percutaneous balloon angioplasty was performed in five patients (29.4%), while stenting was performed in the remaining 12 patients (70.6%). The stenosis-free primary patency rate and freedom from reintervention rate were 76.5% and 88.2%, respectively. The median follow-up was 19.6 months with 88.2% graft survival. There were no mortalities throughout the follow-up period. Serum creatinine levels decreased significantly from 186 mmol/L (range, 148-310 mmol/L) preoperatively to 160 mmol/L (range, 127-236 mmol/L at discharge (P [ .0036). The glomerular filtration rates increased from 32.1 mL/min (range, 21.4-45.8 mL/min) to 41.7 mL/min (range, 27.5-52.4 mL/min; P [ .004). Systolic and diastolic blood pressure varied from 140 mm Hg (range, 137-157 mm Hg) and 75 mm Hg (range, 70-80 mm Hg), to 135 mm Hg (range, 130-147 mm Hg and 80 mm Hg (range, 73-80 mm Hg), respectively (P [ .11 and P [ .36). The preoperative number of antihypertensive medications was 2 (range, 1-3) and remained unchanged (P [ .33). Conclusions: The endovascular management of TRAS is safe and presents a high rate of technical success with low morbidity. Its impact on serum creatinine levels is significant in our experience. However, the blood pressure items do not seem to improve postoperatively. (J Vasc Surg 2014;59:1058-65.)
Transplant renal artery stenosis (TRAS) is a rare event that might occur at any time during the postoperative period and follow-up. The incidence of TRAS seems to neighbor 0.8%, and it is a serious predictor of graft loss.1 There is still controversy regarding the potential benefits of endovascular treatment of these lesions in terms of graft survival, improvement in renal function, and blood pressure normalization. The aim of this study is to assess the short- and midterm outcomes of TRAS angioplasty with or without stenting based on a single-center experience. METHODS All patients were referred to our institution from other medical establishments, mainly nephrology units, following a clinical diagnosis of TRAS confirmed by postoperative Doppler ultrasonography. We performed a retrospective From the Department of Vascular Surgery, Institut Mutualiste Montsouris. Author conflict of interest: none. Reprint requests: Joseph Touma, MD, Department of Vascular Surgery, Institut Mutualiste Montsouris, 42 Boulevard Jourdan, Paris, France (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214/$36.00 Copyright Ó 2014 by the Society for Vascular Surgery. http://dx.doi.org/10.1016/j.jvs.2013.10.072
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review of all cases of TRAS treatment from January 2009 to December 2012, based on postoperative reports database, and completed with data from the PMSI (Programme Médicalisé des Systèmes d'Information) French national database, where all admitted patients are registered. We collected data concerning patients’ characteristics (age, gender, comorbidities), organ donors’ characteristics, type of anastomosis, clinical presentation, time to presentation, type of procedure (angioplasty with or without stent placement, type and number of stents), early and late outcomes, and serum creatinine levels and blood pressure value before the procedure, at discharge, and at the latest follow-up. We updated our information by contacting the referent nephrologist of each patient. Operative technique. All endovascular procedures took place in the operating theater that is equipped with OEC 9900 Elite mobile C-arm (GE Healthcare, Chalfont St. Giles, Buckinghamshire, UK). The transplant renal artery was implanted on the external iliac artery using an end-to-side anastomosis in all treated patients. Under local or general anesthesia, a percutaneous ultrasoundguided retrograde femoral access, ipsilateral to the graft, was performed using a 5F short sheath. At this stage, all patients received intravenous heparin sodium (50 IU/kg). A preliminary nonselective angiography was first performed in order to confirm the diagnosis, rule out iliac obstructive disease, and determine the orientation of the C-arm that
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allowed an optimal exposition of the transplant artery, generally through a 30 to 45 left rotation in the transverse plane. When the stenosis was confirmed, catheterization of the renal artery was performed using a 0.035” or a 0.014” guidewire and different-shaped catheters (5F Vanschie 1, 2, or 3 catheters; Cook, Bloomington, Ind; and 5F Bern catheter; Boston Scientific, Natick, Mass). Subsequently, the balloon catheter and/or balloon-expandable monorail stent system was inserted and deployed. Road-mapping allowed minimum usage of contrast material. Stenosis measurement was based on the ratio between the narrowed segment and the following normal segment of the renal artery. A stenosis was considered significant when superior to 70%, especially when ultrasound criteria were present (allograft artery peak systolic velocity >2 m/s). Balloon and stent size were chosen to match the diameter of the normal adjacent segment of the renal artery. After deployment, a completion angiography was performed. The femoral artery hemostasis was obtained by manual compression. Immediate postoperative follow-up was performed in our unit, with close surveillance of clinical features (femoral access, volume status, blood pressure, urine volume) and biological tests (hemoglobin, serum creatinine level). Discharge criteria were the absence of procedure-related complications and decrease or stability of blood pressure and serum creatinine levels. A Doppler ultrasonography was performed before discharge. Further follow-up was conducted by the referring nephrology unit. Doppler ultrasonography was also performed at 1 month, at 6 months, and at any time during follow-up if recurrence was suspected. The primary end point was the stenosis-free primary patency rate. Secondary end points were freedom from reintervention, graft survival, renal function, blood pressure evolution, and number of antihypertensive drugs. Statistical analysis. We used the Kaplan-Meier method to represent the patency rates. Continuous data were expressed as medians with interquartile range (Q1-Q3). We performed a paired two-sample Student t-test to compare preoperative and postoperative levels of serum creatinine and blood pressure. The number of antihypertensive medications was compared with use of the Wilcoxon rank test. The software used for statistical analysis was StatView (SAS Institute Inc). A probability value of .05 was the threshold of statistical significance. RESULTS A total of 17 patients were admitted in our institution with a high clinical suspicion of TRAS and positive duplex ultrasound findings, including allograft artery peak systolic velocity of 270 (200-450) cm/sec. There were 10 men and seven women, with a median age of 65 years (range, 55-68 years). The etiology of the original renal disease was diabetic nephropathy (n ¼ 5), hypertensive nephropathy (n ¼ 3), hepato-renal or renal polykystosis (n ¼ 2), Berger disease (n ¼ 2), systemic lupus (n ¼ 1); reno-vascular disease (n ¼ 1), chronic interstitial nephropathy (n ¼ 1),
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nephroblastoma with bilateral nephrectomy (n ¼ 1), and one unknown origin. The prerenal transplant median systolic and diastolic blood pressure values were, respectively, 150 mm Hg (range, 146-157 mm Hg) and 88 mm Hg (range, 82-97 mm Hg). Clinical presentation was delayed graft function in five cases, secondary graft function deterioration in nine cases, acute hypertension in one case, acute pulmonary edema in one case, and severe duplex abnormalities without clinical dysfunction in one case. Three patients received renal grafts from living donors, while the 14 others received allografts from brain-deceased patients. The patients’ characteristics are compiled in the Table. In all patients, end-to-side anastomosis with use of the external iliac was performed. The median time from renal transplantation to presentation was 40 days (range, 15-90 days). Six patients (35.2%) presented and were treated within the first 2 weeks after transplantation (Fig 1). One patient had returned to hemodialysis at admission. In all remaining patients, the nadir post-transplant serum creatinine level was 160 mmol/L (range, 116-181 mmol/L), while the serum creatinine value at admission was 186 mmol/L (range, 148-310 mmol/L). The stenosis was located in the ostial (n ¼ 5), juxtaostial (n ¼ 7; Fig 2), middle (n ¼ 4), and divided (n ¼ 1) segment of the allograft renal artery and on both renal and external iliac arteries in three patients (Fig 3). The stenosis was confirmed by angiography in all patients. In five patients (29%), only balloon angioplasty was performed, including one kissing-balloon dilatation technique for a stenosis of the allograft artery bifurcation. The 12 other patients were stented using bare-metal balloon-expandable monorail stent systems. Sixteen stents were used: 13 Herculink Elite renal stent (Abbott Vascular), 2 Monorail Liberte coronary stents (Boston Scientific), and 1 Omnilink Elite stent (Abbott Vascular) in an external iliac artery. The median stent diameter was 5 mm (range, 5-6 mm), and the median stent length was 15 mm (range, 12-18 mm). No intraoperative complications were observed. In two patients, the obstacle was due to a kink of the artery distal to the anastomosis and resolved after stenting. All other patients presented with classic stenosis appearing as linear reduction of the vessel lumen. Early postoperative outcomes. Early postoperative events (ie, prior to day 30) were marked by four early restenosis (
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Table. Patients’ characteristics, presentation, and management Living/ Interval between Patient Age, deceased transplantation No. years Gender Original renal disease donor and treatment
Clinical presentation
Type of procedure
Complication Restenosis Renal artery dissectionþ stent misplacement Restenosis -
1 2 3
54 19 65
Male Renal polykystosis Female Bilateral nephrectomy Male Berger disease
D L L
49 days 15 days 12 days
Delayed graft function Secondary renal failure Secondary renal failure
Angioplasty Angioplasty Stent placement
4 5 6 7
65 67 62 60
Male Male Female Female
D D D D
24 days 9 days 16 days 75 days
Secondary renal failure Secondary renal failure Delayed graft function Secondary renal failure
Stent Stent Stent Stent
8
66
D
158 days
Secondary renal failure
Angioplasty
9
61
Diabetic nephropathy Diabetic nephropathy Reno-vascular disease Hypertensive nephropathy Female Chronic interstitial nephropathy Female Diabetic nephropathy
L
40 days
10
75
Male
Diabetic nephropathy
D
122 days
11
44
Male
D
90 days
-
12 13
41 71
D D
74 days 10 years
Secondary renal failure Stent placement Acute pulmonary edema Angioplasty
Restenosis -
14 15 16 17
55 68 71 68
Hepato-renal polykystosis Female Systemic lupus Male Hypertensive nephropathy Male Berger disease Male Diabetic nephropathy Male Undetermined Female Hypertensive nephropathy
Secondary renal failure/ Stent placement hemodialysis None/Doppler Stent placement ultrasound findings Delayed graft function Angioplasty
D D D D
6 days 240 days 15 days 12 days
Delayed graft function Secondary renal failure Delayed graft function Severe hypertension
Stent Stent Stent Stent
placement placement placement placement
-
placement placement placement placement
-
D, Deceased; L, living.
Fig 1. Intraoperative angiography. A, Early post-transplantation distal stenosis of the renal transplant artery, at day 6. B, Satisfactory diameter retrieval after stenting.
procedures were uncomplicated. The overall technical success rate was 88.2% (15/17) when considering restenosis events requiring redo intervention. The serum creatinine level after endovascular treatment, at discharge, was 160 mmol/L (range, 127-236 mmol/L). There was a significant decrease in serum creatinine levels (P ¼ .0036). The glomerular filtration rates increased from 32.1 mL/min (range, 21.4-45.8 mL/min) to 41.7 mL/min (range, 27.5-52.4 mL/min; P ¼ .004; Fig 4).
The systolic blood pressure decreased from 140 mm Hg (range, 137-157 mm Hg) before the procedure, to 135 mm Hg (range, 130-147 mm Hg) at discharge (Fig 5). This result was not significant (P ¼ .11). The mean diastolic blood pressure was not significantly different before the procedure and at discharge, slightly increasing from 75 mm Hg (range, 70-80 mm Hg) to 80 mm Hg (range, 73-80 mm Hg; P ¼.36). There was no immediate modification of the number of antihypertensive drugs in all patients.
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Fig 2. A, Postostial long stenosis of the renal transplant artery. B, Satisfactory result after stenting.
Late postoperative outcomes. The stenosis-free primary patency and freedom from reintervention curves are represented in Fig 6, a and b. No postoperative deaths occurred. Two renal transplants were extracted 10 and 22 months after the endovascular procedure, because of persistent renal insufficiency in the patient who had been under hemodialysis since the early post-transplant period, and chronic rejection in the other case. Of the remaining transplants, four suffered from additional nonvascular renal disease that altered the graft function: one graft tuberculosis, one lupic nephropathy, one glomerulopathy with severe lesions of focal segmental hyalinosis, and one graft function alteration after multiple dehydration episodes. The serum creatinine level in all patients that have kept their graft was 180 mmol/L (range, 135-292 mmol/L) at latest follow-up. Only two patients had a reduction of the number of antihypertensive drugs by half. The median number of antihypertensive drugs remained unchanged with median two antihypertensive medications (range, 1-3) and no significant difference when compared with preoperative condition (P ¼ .33). Concerning the single patient who presented with acute hypertension, the blood pressure diminished from 165/85 mm Hg to 150/ 75 mm Hg, and one antihypertensive drug was pursued instead of bitherapy. The patients who underwent redo stenting maintained the patency of the renal transplant artery. None of the early managed patients (
The median follow-up was 19.6 months (range, 8.524 months), and the mean follow-up was 18.5 6 8.5 months. DISCUSSION This retrospective study highlights the safety of the endovascular management of TRAS, including treatment of early TRAS, its efficiency concerning cases presenting with graft function alteration, the inconstant reduction of mean blood pressure values, and the non-negligible rate of restenosis, being, however, simply and successfully managed. TRAS is a serious complication of renal transplantation, with an incidence reaching 0.8%, with most cases occurring during the first 6 months and in elderly transplanted patients.1 Early appearing stenoses are mainly due to traumatic intimal injury during harvesting or vessel manipulation, kinking of the artery when it is longer than the vein, or technical problems with the vascular suture, while stenoses occurring later, sometimes in terms of years, reflect allograft renal artery hyperplasia or renal and/or iliac atherosclerotic evolution.2 Late and diffuse stenosis might also reflect endothelial damage related to immune response.3 In our series, the median time to presentation was 40 days, and 13 (76.4%) patients presented before day 90. This result suggests that the vessel stenosis was most probably related to a technical problem. Clinical indicators of TRAS are graft dysfunction and/ or new or refractory hypertension.
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Fig 3. Intraoperative angiography. A, Severe iliac lesion probably resulting from clamp application, associated to juxtaostial transplant artery stenosis. B, Both lesions were successfully stented.
Fig 4. Evolution of serum creatinine levels (A) and glomerular filtration rates (B) expressed as medians with interquartile range. FU, Follow-up; RT, renal transplantation.
The most often retained Doppler ultrasonography criteria for TRAS are peak systolic velocity higher than 200 cm/sec, resistance index <0.5, and velocity gradient >2:1.4-6 Reported significant risk factors for TRAS are delayed graft function1,7,8 and cytomegalovirus infection.7-9 Other risk factors are inconstantly significant: expanded donor criteria (mainly regarding age),1 obesity,8 and ischemic
heart disease.1 The origin of the graft is also an uncertain risk factor: a deceased donor is not significantly correlated with TRAS according to some series.1,7,10 On the other hand, prevalence rates of TRAS in deceased donor transplants have been reported to reach 4.1%, 4.5%, and 6.5%,11-13 compared with 0.3%, 0.8%, and 1.7% in living related transplants.11,14,15
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Fig 5. Evolution of systolic (A) and diastolic (B) blood pressure expressed as medians with interquartile range. FU, Follow-up; RT, renal transplantation.
Fig 6. Kaplan-Meier curves for stenosis-free primary patency (a) and freedom from reintervention rates (b). The arrow indicates the time where standard error (SE) exceeds 10%.
The presence of clinical and/or biological symptoms must be the main indication of treatment. An isolated Doppler ultrasonography examination showing proximal stenosis of the allograft artery does not always imply clinical consequence. Interestingly, a recent study describes severely elevated velocities in nearly 45% of transplanted patients (>400 cm/sec) with normal clinical course or normalization of the peak systolic velocity in the majority of cases without intervention. Only those with a persistent elevated value of the peak systolic velocity were directed to angiography, with time to angiography varying from 1 week to 4 months.16 Two therapeutic approaches are possible: revision open surgery is actually considered as a rescue therapy and is reserved for cases of unsuccessful angioplasty or with severe complicated stenosis, because of the high reported rate of significant complications such as graft loss (15% to 20%), ureteral injury, and reoperation.17 The vast majority of TRAS cases are treated using an endovascular approach, either by balloon angioplasty, or by
primary or secondary stenting, that typically address linear short lesions relatively distal from the anastomosis site. However, in spite of the lower effectiveness and the higher risk of percutaneous transluminal angioplasty in anastomotic lesions,17,18 many authors report an uneventful treatment of stenosis at the anastomotic line6,19,20 with a delay to percutaneous transluminal angioplasty of at least 2 months post-transplantation.6 In our study, four lesions were located at the anastomotic site, and 13 were distal to the anastomosis, with one hilar lesion requiring a kissing-balloon technique. None of the anastomotic dilatation procedures induced postoperative complications, including those performed early after transplantation (35%). In our opinion, the decision of early TRAS endovascular management especially for anastomotic lesions should take into account the patients’ post-transplant general condition and implies a vascular surgeon performing the procedure in an operating room in the presence of an anesthesiologist, after appropriate patient installation.
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Endovascular treatment of TRAS has proved to be feasible, with a technical success rate frequently reported between 89%5,11,21 and 100%,3,4,22 which is coherent with the overall technical success rate of 88.2% in this series. It is also a safe technique, with a specific complication rate varying in recent series from 0%3,4,6 to 5.5%.5,22 Peregrin et al noticeably report an overall complication rate of 25.5% that includes medically managed groin hematoma, and intraoperatively stented iatrogenic renal dissection, all managed successfully without sequelae. Restenosis is the main inherent complication of the endovascular techniques, with no specificity regarding the particular location at the renal transplant artery. Balloon angioplasty alone entails a 10% to 56% restenosis rate.7,11,14,18,23 This result seems to improve with stent usage, with rates of restenosis following primary stenting varying from 5.5%4 to 20%.23 In our series, four patients presented with duplex signs of transplant artery stenosis during the early postoperative period (ie, prior to day 30). One patient had been treated with balloon angioplasty alone and was therefore subsequently stented. In the three remaining patients, TRAS had been initially stented. The restenosis was confirmed but moderate in two patients, and was therefore medically managed with good outcomes. In the remaining case, the signs were in fact related to the same persistent proximal stenosis because of an incomplete coverage of the lesion by the stent. Consequently, the freedom from reintervention rate was 88.2%. No late restenosis was observed during the available follow-up. Effectiveness of angioplasty in terms of graft survival is equivocal. Audard et al7 reported a long-term graft survival significantly higher in TRAS-free transplanted patients, compared with the TRAS group, despite angioplasty. Hurst et al stated that graft survival after TRAS was not significantly different in patients treated with angioplasty compared with those without angioplasty. Conversely, multiple series4,24,25 report no difference in the survival curve of the grafts without TRAS compared with those with stenting treated with TRAS. Another ambiguity is found concerning endovascular treatment effectiveness in improving hypertension and reducing antihypertensive medication doses. Although we observe a trend toward a positive impact on lowering systolic or diastolic blood pressure and the number of drugs postoperatively, this is not statistically significant in our series. This may be due to the relatively small size of this series and the fact that most patients have no signs of acute or novel hypertension at admission. Some published series report significant decrease of the blood pressure values as well as the number of antihypertensive drugs,4,22 while others rejoin our experience, obtaining nonsignificant change of those values.26,27 The impact on postoperative creatinine levels seems more consensual, with a majority of reports citing significant decrease following angioplasty with or without stent placement.3-6,11,22 Our study is limited by the small number of included patients, the retrospective process, and the absence of a control group of transplanted patients without TRAS,
due to the fact that all treated patients were referred to our center from external transplantation units. CONCLUSIONS The endovascular management of TRAS seems safe and shows a high rate of technical success. Its effectiveness on serum creatinine value seems almost constant, but the impact on blood pressure evolution must be further investigated in larger series. One must keep in mind that the ultimate end point is the graft survival. The latter presents heterogeneous outcomes when the actual literature is reviewed, in the absence of prospective controlled studies. AUTHOR CONTRIBUTIONS Conception and design: JT, AC, MC Analysis and interpretation: JT, AC Data collection: JT Writing the article: JT Critical revision of the article: AC, BB, FA, MC Final approval of the article: JT, AC, BB, FA, MC Statistical analysis: JT Obtained funding: Not applicable Overall responsibility: JT REFERENCES 1. Hurst FP, Abbott KC, Neff RT, Elster EA, Falta EM, Lentine KL, et al. Incidence, predictors and outcomes of transplant renal artery stenosis after kidney transplantation: analysis of USRDS. Am J Nephrol 2009;30:459-67. 2. Becker BN, Odorico JS, Becker YT, Leverson G, McDermott JC, Grist T, et al. Peripheral vascular disease and renal transplant artery stenosis: a reappraisal of transplant renovascular disease. Clin Transplant 1999;13:349-55. 3. Pappas P, Zavos G, Kaza S, Leonardou P, Theodoropoulou E, Bokos J, et al. Angioplasty and stenting of arterial stenosis affecting renal transplant function. Transplant Proc 2008;40:1391-6. 4. Su CH, Lian JD, Chang HR, Wu SW, Chen SC, Tsai CF, et al. Longterm outcomes of patients treated with primary stenting for transplant renal artery stenosis: a 10-year case cohort study. World J Surg 2012;36:222-8. 5. Marini M, Fernandez-Rivera C, Cao I, Gulias D, Alonso A, LopezMuniz A, et al. Treatment of transplant renal artery stenosis by percutaneous transluminal angioplasty and/or stenting: study in 63 patients in a single institution. Transplant Proc 2011;43:2205-7. 6. Sharma S, Potdar A, Kulkarni A. Percutaneous transluminal renal stenting for transplant renal artery stenosis. Catheter Cardiovasc Interv 2011;77:287-93. 7. Audard V, Matignon M, Hemery F, Snanoudj R, Desgranges P, Anglade MC, et al. Risk factors and long-term outcome of transplant renal artery stenosis in adult recipients after treatment by percutaneous transluminal angioplasty. Am J Transplant 2006;6:95-9. 8. Kamali K, Abbasi MA, Behzadi AH, Mortazavi A, Bastani B. Incidence and risk factors of transplant renal artery stenosis in living unrelated donor renal transplantation. J Ren Care 2010;36:149-52. 9. Pouria S, State OI, Wong W, Hendry BM. CMV infection is associated with transplant renal artery stenosis. QJM 1998;91:185-9. 10. Fauchald P, Vatne K, Paulsen D, Brodahl U, Sodal G, Holdaas H, et al. Long-term clinical results of percutaneous transluminal angioplasty in transplant renal artery stenosis. Nephrol Dial Transplant 1992;7:256-9. 11. Patel NH, Jindal RM, Wilkin T, Rose S, Johnson MS, Shah H, et al. Renal arterial stenosis in renal allografts: retrospective study of predisposing factors and outcome after percutaneous transluminal angioplasty. Radiology 2001;219:663-7.
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12. Halimi JM, Al-Najjar A, Buchler M, Birmele B, Tranquart F, Alison D, et al. Transplant renal artery stenosis: potential role of ischemia/ reperfusion injury and long-term outcome following angioplasty. J Urol 1999;161:28-32. 13. Rengel M, Gomes-Da-Silva G, Inchaustegui L, Lampreave JL, Robledo R, Echenagusia A, et al. Renal artery stenosis after kidney transplantation: diagnostic and therapeutic approach. Kidney Int 1998;68(Suppl):S99-106. 14. Sankari BR, Geisinger M, Zelch M, Brouhard B, Cunningham R, Novick AC. Post-transplant renal artery stenosis: impact of therapy on long-term kidney function and blood pressure control. J Urol 1996;155:1860-4. 15. Mammen NI, Chacko N, Ganesh G, Jacob CK, Shastry JC, Pandey AP. Aspects of hypertension in renal allograft recipients. A study of 1000 live renal transplants. Br J Urol 1993;71:256-8. 16. Siskind E, Lombardi P, Blum M, Tyrell R, Villa M, Kuncewitch M, et al. Significance of elevated transplant renal artery velocities in the postoperative renal transplant patient. Clin Transplant 2013;27: e157-60. 17. Merkus JW, Huysmans FT, Hoitsma AJ, Buskens FG, Skotnicki SH. Koene RA. Renal allograft artery stenosis: results of medical treatment and intervention. A retrospective analysis. Transpl Int 1993;6:111-5. 18. Chandrasoma P, Aberle AM. Anastomotic line renal artery stenosis after transplantation. J Urol 1986;135:1159-62. 19. Greenstein SM, Verstandig A, McLean GK, DaFoe DC, Burke DR, Meranze SG, et al. Percutaneous transluminal angioplasty: the procedure of choice for renal allograft artery stenosis. Transplant Proc 1987;19:2194-6.
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20. Matalon TA, Thompson MJ, Patel SK, Brunner MC, Merkel FK, Jensik SC. Percutaneous transluminal angioplasty for transplant renal artery stenosis. J Vasc Interv Radiol 1992;3:55-8. 21. Peregrin JH, Stribrna J, Lacha J, Skibova J. Long-term follow-up of renal transplant patients with renal artery stenosis treated by percutaneous angioplasty. Eur J Radiol 2008;66:512-8. 22. Beecroft JR, Rajan DK, Clark TW, Robinette M, Stavropoulos SW. Transplant renal artery stenosis: outcome after percutaneous intervention. J Vasc Interv Radiol 2004;15:1407-13. 23. Voiculescu A, Schmitz M, Hollenbeck M, Braasch S, Luther B, Sandmann W, et al. Management of arterial stenosis affecting kidney graft perfusion: a single-centre study in 53 patients. Am J Transplant 2005;5:1731-8. 24. Valpreda S, Messina M, Rabbia C. Stenting of transplant renal artery stenosis: outcome in a single center study. J Cardiovasc Surg (Torino) 2008;49:565-70. 25. Salvadori M, Di Maria L, Rosati A, Larti A, Piperno R, Becherelli P, et al. Efficacy and safety of Palmaz stent implantation in the treatment of renal artery stenosis in renal transplantation. Transplant Proc 2005;37:1047-8. 26. Geddes CC, McManus SK, Koteeswaran S, Baxter GM. Long-term outcome of transplant renal artery stenosis managed conservatively or by radiological intervention. Clin Transplant 2008;22:572-8. 27. Wong W, Fynn SP, Higgins RM, Walters H, Evans S, Deane C, et al. Transplant renal artery stenosis in 77 patientsedoes it have an immunological cause? Transplantation 1996;61:215-9. Submitted Jul 23, 2013; accepted Oct 10, 2013.
Transplant renal artery stenosis (TRAS) is a rare event that might occur at any time during the postoperative period and follow-up. The incidence of TRAS seems to neighbor 0.8%, and it is a serious predictor of graft loss.1 There is still controversy regarding the potential benefits of endovascular treatment of these lesions in terms of graft survival, improvement in renal function, and blood pressure normalization. The aim of this study is to assess the short- and midterm outcomes of TRAS angioplasty with or without stenting based on a single-center experience. METHODS All patients were referred to our institution from other medical establishments, mainly nephrology units, following a clinical diagnosis of TRAS confirmed by postoperative Doppler ultrasonography. We performed a retrospective From the Department of Vascular Surgery, Institut Mutualiste Montsouris. Author conflict of interest: none. Reprint requests: Joseph Touma, MD, Department of Vascular Surgery, Institut Mutualiste Montsouris, 42 Boulevard Jourdan, Paris, France (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214/$36.00 Copyright Ó 2014 by the Society for Vascular Surgery. http://dx.doi.org/10.1016/j.jvs.2013.10.072
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review of all cases of TRAS treatment from January 2009 to December 2012, based on postoperative reports database, and completed with data from the PMSI (Programme Médicalisé des Systèmes d'Information) French national database, where all admitted patients are registered. We collected data concerning patients’ characteristics (age, gender, comorbidities), organ donors’ characteristics, type of anastomosis, clinical presentation, time to presentation, type of procedure (angioplasty with or without stent placement, type and number of stents), early and late outcomes, and serum creatinine levels and blood pressure value before the procedure, at discharge, and at the latest follow-up. We updated our information by contacting the referent nephrologist of each patient. Operative technique. All endovascular procedures took place in the operating theater that is equipped with OEC 9900 Elite mobile C-arm (GE Healthcare, Chalfont St. Giles, Buckinghamshire, UK). The transplant renal artery was implanted on the external iliac artery using an end-to-side anastomosis in all treated patients. Under local or general anesthesia, a percutaneous ultrasoundguided retrograde femoral access, ipsilateral to the graft, was performed using a 5F short sheath. At this stage, all patients received intravenous heparin sodium (50 IU/kg). A preliminary nonselective angiography was first performed in order to confirm the diagnosis, rule out iliac obstructive disease, and determine the orientation of the C-arm that
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allowed an optimal exposition of the transplant artery, generally through a 30 to 45 left rotation in the transverse plane. When the stenosis was confirmed, catheterization of the renal artery was performed using a 0.035” or a 0.014” guidewire and different-shaped catheters (5F Vanschie 1, 2, or 3 catheters; Cook, Bloomington, Ind; and 5F Bern catheter; Boston Scientific, Natick, Mass). Subsequently, the balloon catheter and/or balloon-expandable monorail stent system was inserted and deployed. Road-mapping allowed minimum usage of contrast material. Stenosis measurement was based on the ratio between the narrowed segment and the following normal segment of the renal artery. A stenosis was considered significant when superior to 70%, especially when ultrasound criteria were present (allograft artery peak systolic velocity >2 m/s). Balloon and stent size were chosen to match the diameter of the normal adjacent segment of the renal artery. After deployment, a completion angiography was performed. The femoral artery hemostasis was obtained by manual compression. Immediate postoperative follow-up was performed in our unit, with close surveillance of clinical features (femoral access, volume status, blood pressure, urine volume) and biological tests (hemoglobin, serum creatinine level). Discharge criteria were the absence of procedure-related complications and decrease or stability of blood pressure and serum creatinine levels. A Doppler ultrasonography was performed before discharge. Further follow-up was conducted by the referring nephrology unit. Doppler ultrasonography was also performed at 1 month, at 6 months, and at any time during follow-up if recurrence was suspected. The primary end point was the stenosis-free primary patency rate. Secondary end points were freedom from reintervention, graft survival, renal function, blood pressure evolution, and number of antihypertensive drugs. Statistical analysis. We used the Kaplan-Meier method to represent the patency rates. Continuous data were expressed as medians with interquartile range (Q1-Q3). We performed a paired two-sample Student t-test to compare preoperative and postoperative levels of serum creatinine and blood pressure. The number of antihypertensive medications was compared with use of the Wilcoxon rank test. The software used for statistical analysis was StatView (SAS Institute Inc). A probability value of .05 was the threshold of statistical significance. RESULTS A total of 17 patients were admitted in our institution with a high clinical suspicion of TRAS and positive duplex ultrasound findings, including allograft artery peak systolic velocity of 270 (200-450) cm/sec. There were 10 men and seven women, with a median age of 65 years (range, 55-68 years). The etiology of the original renal disease was diabetic nephropathy (n ¼ 5), hypertensive nephropathy (n ¼ 3), hepato-renal or renal polykystosis (n ¼ 2), Berger disease (n ¼ 2), systemic lupus (n ¼ 1); reno-vascular disease (n ¼ 1), chronic interstitial nephropathy (n ¼ 1),
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nephroblastoma with bilateral nephrectomy (n ¼ 1), and one unknown origin. The prerenal transplant median systolic and diastolic blood pressure values were, respectively, 150 mm Hg (range, 146-157 mm Hg) and 88 mm Hg (range, 82-97 mm Hg). Clinical presentation was delayed graft function in five cases, secondary graft function deterioration in nine cases, acute hypertension in one case, acute pulmonary edema in one case, and severe duplex abnormalities without clinical dysfunction in one case. Three patients received renal grafts from living donors, while the 14 others received allografts from brain-deceased patients. The patients’ characteristics are compiled in the Table. In all patients, end-to-side anastomosis with use of the external iliac was performed. The median time from renal transplantation to presentation was 40 days (range, 15-90 days). Six patients (35.2%) presented and were treated within the first 2 weeks after transplantation (Fig 1). One patient had returned to hemodialysis at admission. In all remaining patients, the nadir post-transplant serum creatinine level was 160 mmol/L (range, 116-181 mmol/L), while the serum creatinine value at admission was 186 mmol/L (range, 148-310 mmol/L). The stenosis was located in the ostial (n ¼ 5), juxtaostial (n ¼ 7; Fig 2), middle (n ¼ 4), and divided (n ¼ 1) segment of the allograft renal artery and on both renal and external iliac arteries in three patients (Fig 3). The stenosis was confirmed by angiography in all patients. In five patients (29%), only balloon angioplasty was performed, including one kissing-balloon dilatation technique for a stenosis of the allograft artery bifurcation. The 12 other patients were stented using bare-metal balloon-expandable monorail stent systems. Sixteen stents were used: 13 Herculink Elite renal stent (Abbott Vascular), 2 Monorail Liberte coronary stents (Boston Scientific), and 1 Omnilink Elite stent (Abbott Vascular) in an external iliac artery. The median stent diameter was 5 mm (range, 5-6 mm), and the median stent length was 15 mm (range, 12-18 mm). No intraoperative complications were observed. In two patients, the obstacle was due to a kink of the artery distal to the anastomosis and resolved after stenting. All other patients presented with classic stenosis appearing as linear reduction of the vessel lumen. Early postoperative outcomes. Early postoperative events (ie, prior to day 30) were marked by four early restenosis (
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Table. Patients’ characteristics, presentation, and management Living/ Interval between Patient Age, deceased transplantation No. years Gender Original renal disease donor and treatment
Clinical presentation
Type of procedure
Complication Restenosis Renal artery dissectionþ stent misplacement Restenosis -
1 2 3
54 19 65
Male Renal polykystosis Female Bilateral nephrectomy Male Berger disease
D L L
49 days 15 days 12 days
Delayed graft function Secondary renal failure Secondary renal failure
Angioplasty Angioplasty Stent placement
4 5 6 7
65 67 62 60
Male Male Female Female
D D D D
24 days 9 days 16 days 75 days
Secondary renal failure Secondary renal failure Delayed graft function Secondary renal failure
Stent Stent Stent Stent
8
66
D
158 days
Secondary renal failure
Angioplasty
9
61
Diabetic nephropathy Diabetic nephropathy Reno-vascular disease Hypertensive nephropathy Female Chronic interstitial nephropathy Female Diabetic nephropathy
L
40 days
10
75
Male
Diabetic nephropathy
D
122 days
11
44
Male
D
90 days
-
12 13
41 71
D D
74 days 10 years
Secondary renal failure Stent placement Acute pulmonary edema Angioplasty
Restenosis -
14 15 16 17
55 68 71 68
Hepato-renal polykystosis Female Systemic lupus Male Hypertensive nephropathy Male Berger disease Male Diabetic nephropathy Male Undetermined Female Hypertensive nephropathy
Secondary renal failure/ Stent placement hemodialysis None/Doppler Stent placement ultrasound findings Delayed graft function Angioplasty
D D D D
6 days 240 days 15 days 12 days
Delayed graft function Secondary renal failure Delayed graft function Severe hypertension
Stent Stent Stent Stent
placement placement placement placement
-
placement placement placement placement
-
D, Deceased; L, living.
Fig 1. Intraoperative angiography. A, Early post-transplantation distal stenosis of the renal transplant artery, at day 6. B, Satisfactory diameter retrieval after stenting.
procedures were uncomplicated. The overall technical success rate was 88.2% (15/17) when considering restenosis events requiring redo intervention. The serum creatinine level after endovascular treatment, at discharge, was 160 mmol/L (range, 127-236 mmol/L). There was a significant decrease in serum creatinine levels (P ¼ .0036). The glomerular filtration rates increased from 32.1 mL/min (range, 21.4-45.8 mL/min) to 41.7 mL/min (range, 27.5-52.4 mL/min; P ¼ .004; Fig 4).
The systolic blood pressure decreased from 140 mm Hg (range, 137-157 mm Hg) before the procedure, to 135 mm Hg (range, 130-147 mm Hg) at discharge (Fig 5). This result was not significant (P ¼ .11). The mean diastolic blood pressure was not significantly different before the procedure and at discharge, slightly increasing from 75 mm Hg (range, 70-80 mm Hg) to 80 mm Hg (range, 73-80 mm Hg; P ¼.36). There was no immediate modification of the number of antihypertensive drugs in all patients.
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Fig 2. A, Postostial long stenosis of the renal transplant artery. B, Satisfactory result after stenting.
Late postoperative outcomes. The stenosis-free primary patency and freedom from reintervention curves are represented in Fig 6, a and b. No postoperative deaths occurred. Two renal transplants were extracted 10 and 22 months after the endovascular procedure, because of persistent renal insufficiency in the patient who had been under hemodialysis since the early post-transplant period, and chronic rejection in the other case. Of the remaining transplants, four suffered from additional nonvascular renal disease that altered the graft function: one graft tuberculosis, one lupic nephropathy, one glomerulopathy with severe lesions of focal segmental hyalinosis, and one graft function alteration after multiple dehydration episodes. The serum creatinine level in all patients that have kept their graft was 180 mmol/L (range, 135-292 mmol/L) at latest follow-up. Only two patients had a reduction of the number of antihypertensive drugs by half. The median number of antihypertensive drugs remained unchanged with median two antihypertensive medications (range, 1-3) and no significant difference when compared with preoperative condition (P ¼ .33). Concerning the single patient who presented with acute hypertension, the blood pressure diminished from 165/85 mm Hg to 150/ 75 mm Hg, and one antihypertensive drug was pursued instead of bitherapy. The patients who underwent redo stenting maintained the patency of the renal transplant artery. None of the early managed patients (
The median follow-up was 19.6 months (range, 8.524 months), and the mean follow-up was 18.5 6 8.5 months. DISCUSSION This retrospective study highlights the safety of the endovascular management of TRAS, including treatment of early TRAS, its efficiency concerning cases presenting with graft function alteration, the inconstant reduction of mean blood pressure values, and the non-negligible rate of restenosis, being, however, simply and successfully managed. TRAS is a serious complication of renal transplantation, with an incidence reaching 0.8%, with most cases occurring during the first 6 months and in elderly transplanted patients.1 Early appearing stenoses are mainly due to traumatic intimal injury during harvesting or vessel manipulation, kinking of the artery when it is longer than the vein, or technical problems with the vascular suture, while stenoses occurring later, sometimes in terms of years, reflect allograft renal artery hyperplasia or renal and/or iliac atherosclerotic evolution.2 Late and diffuse stenosis might also reflect endothelial damage related to immune response.3 In our series, the median time to presentation was 40 days, and 13 (76.4%) patients presented before day 90. This result suggests that the vessel stenosis was most probably related to a technical problem. Clinical indicators of TRAS are graft dysfunction and/ or new or refractory hypertension.
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Fig 3. Intraoperative angiography. A, Severe iliac lesion probably resulting from clamp application, associated to juxtaostial transplant artery stenosis. B, Both lesions were successfully stented.
Fig 4. Evolution of serum creatinine levels (A) and glomerular filtration rates (B) expressed as medians with interquartile range. FU, Follow-up; RT, renal transplantation.
The most often retained Doppler ultrasonography criteria for TRAS are peak systolic velocity higher than 200 cm/sec, resistance index <0.5, and velocity gradient >2:1.4-6 Reported significant risk factors for TRAS are delayed graft function1,7,8 and cytomegalovirus infection.7-9 Other risk factors are inconstantly significant: expanded donor criteria (mainly regarding age),1 obesity,8 and ischemic
heart disease.1 The origin of the graft is also an uncertain risk factor: a deceased donor is not significantly correlated with TRAS according to some series.1,7,10 On the other hand, prevalence rates of TRAS in deceased donor transplants have been reported to reach 4.1%, 4.5%, and 6.5%,11-13 compared with 0.3%, 0.8%, and 1.7% in living related transplants.11,14,15
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Fig 5. Evolution of systolic (A) and diastolic (B) blood pressure expressed as medians with interquartile range. FU, Follow-up; RT, renal transplantation.
Fig 6. Kaplan-Meier curves for stenosis-free primary patency (a) and freedom from reintervention rates (b). The arrow indicates the time where standard error (SE) exceeds 10%.
The presence of clinical and/or biological symptoms must be the main indication of treatment. An isolated Doppler ultrasonography examination showing proximal stenosis of the allograft artery does not always imply clinical consequence. Interestingly, a recent study describes severely elevated velocities in nearly 45% of transplanted patients (>400 cm/sec) with normal clinical course or normalization of the peak systolic velocity in the majority of cases without intervention. Only those with a persistent elevated value of the peak systolic velocity were directed to angiography, with time to angiography varying from 1 week to 4 months.16 Two therapeutic approaches are possible: revision open surgery is actually considered as a rescue therapy and is reserved for cases of unsuccessful angioplasty or with severe complicated stenosis, because of the high reported rate of significant complications such as graft loss (15% to 20%), ureteral injury, and reoperation.17 The vast majority of TRAS cases are treated using an endovascular approach, either by balloon angioplasty, or by
primary or secondary stenting, that typically address linear short lesions relatively distal from the anastomosis site. However, in spite of the lower effectiveness and the higher risk of percutaneous transluminal angioplasty in anastomotic lesions,17,18 many authors report an uneventful treatment of stenosis at the anastomotic line6,19,20 with a delay to percutaneous transluminal angioplasty of at least 2 months post-transplantation.6 In our study, four lesions were located at the anastomotic site, and 13 were distal to the anastomosis, with one hilar lesion requiring a kissing-balloon technique. None of the anastomotic dilatation procedures induced postoperative complications, including those performed early after transplantation (35%). In our opinion, the decision of early TRAS endovascular management especially for anastomotic lesions should take into account the patients’ post-transplant general condition and implies a vascular surgeon performing the procedure in an operating room in the presence of an anesthesiologist, after appropriate patient installation.
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Endovascular treatment of TRAS has proved to be feasible, with a technical success rate frequently reported between 89%5,11,21 and 100%,3,4,22 which is coherent with the overall technical success rate of 88.2% in this series. It is also a safe technique, with a specific complication rate varying in recent series from 0%3,4,6 to 5.5%.5,22 Peregrin et al noticeably report an overall complication rate of 25.5% that includes medically managed groin hematoma, and intraoperatively stented iatrogenic renal dissection, all managed successfully without sequelae. Restenosis is the main inherent complication of the endovascular techniques, with no specificity regarding the particular location at the renal transplant artery. Balloon angioplasty alone entails a 10% to 56% restenosis rate.7,11,14,18,23 This result seems to improve with stent usage, with rates of restenosis following primary stenting varying from 5.5%4 to 20%.23 In our series, four patients presented with duplex signs of transplant artery stenosis during the early postoperative period (ie, prior to day 30). One patient had been treated with balloon angioplasty alone and was therefore subsequently stented. In the three remaining patients, TRAS had been initially stented. The restenosis was confirmed but moderate in two patients, and was therefore medically managed with good outcomes. In the remaining case, the signs were in fact related to the same persistent proximal stenosis because of an incomplete coverage of the lesion by the stent. Consequently, the freedom from reintervention rate was 88.2%. No late restenosis was observed during the available follow-up. Effectiveness of angioplasty in terms of graft survival is equivocal. Audard et al7 reported a long-term graft survival significantly higher in TRAS-free transplanted patients, compared with the TRAS group, despite angioplasty. Hurst et al stated that graft survival after TRAS was not significantly different in patients treated with angioplasty compared with those without angioplasty. Conversely, multiple series4,24,25 report no difference in the survival curve of the grafts without TRAS compared with those with stenting treated with TRAS. Another ambiguity is found concerning endovascular treatment effectiveness in improving hypertension and reducing antihypertensive medication doses. Although we observe a trend toward a positive impact on lowering systolic or diastolic blood pressure and the number of drugs postoperatively, this is not statistically significant in our series. This may be due to the relatively small size of this series and the fact that most patients have no signs of acute or novel hypertension at admission. Some published series report significant decrease of the blood pressure values as well as the number of antihypertensive drugs,4,22 while others rejoin our experience, obtaining nonsignificant change of those values.26,27 The impact on postoperative creatinine levels seems more consensual, with a majority of reports citing significant decrease following angioplasty with or without stent placement.3-6,11,22 Our study is limited by the small number of included patients, the retrospective process, and the absence of a control group of transplanted patients without TRAS,
due to the fact that all treated patients were referred to our center from external transplantation units. CONCLUSIONS The endovascular management of TRAS seems safe and shows a high rate of technical success. Its effectiveness on serum creatinine value seems almost constant, but the impact on blood pressure evolution must be further investigated in larger series. One must keep in mind that the ultimate end point is the graft survival. The latter presents heterogeneous outcomes when the actual literature is reviewed, in the absence of prospective controlled studies. AUTHOR CONTRIBUTIONS Conception and design: JT, AC, MC Analysis and interpretation: JT, AC Data collection: JT Writing the article: JT Critical revision of the article: AC, BB, FA, MC Final approval of the article: JT, AC, BB, FA, MC Statistical analysis: JT Obtained funding: Not applicable Overall responsibility: JT REFERENCES 1. Hurst FP, Abbott KC, Neff RT, Elster EA, Falta EM, Lentine KL, et al. Incidence, predictors and outcomes of transplant renal artery stenosis after kidney transplantation: analysis of USRDS. Am J Nephrol 2009;30:459-67. 2. Becker BN, Odorico JS, Becker YT, Leverson G, McDermott JC, Grist T, et al. Peripheral vascular disease and renal transplant artery stenosis: a reappraisal of transplant renovascular disease. Clin Transplant 1999;13:349-55. 3. Pappas P, Zavos G, Kaza S, Leonardou P, Theodoropoulou E, Bokos J, et al. Angioplasty and stenting of arterial stenosis affecting renal transplant function. Transplant Proc 2008;40:1391-6. 4. Su CH, Lian JD, Chang HR, Wu SW, Chen SC, Tsai CF, et al. Longterm outcomes of patients treated with primary stenting for transplant renal artery stenosis: a 10-year case cohort study. World J Surg 2012;36:222-8. 5. Marini M, Fernandez-Rivera C, Cao I, Gulias D, Alonso A, LopezMuniz A, et al. Treatment of transplant renal artery stenosis by percutaneous transluminal angioplasty and/or stenting: study in 63 patients in a single institution. Transplant Proc 2011;43:2205-7. 6. Sharma S, Potdar A, Kulkarni A. Percutaneous transluminal renal stenting for transplant renal artery stenosis. Catheter Cardiovasc Interv 2011;77:287-93. 7. Audard V, Matignon M, Hemery F, Snanoudj R, Desgranges P, Anglade MC, et al. Risk factors and long-term outcome of transplant renal artery stenosis in adult recipients after treatment by percutaneous transluminal angioplasty. Am J Transplant 2006;6:95-9. 8. Kamali K, Abbasi MA, Behzadi AH, Mortazavi A, Bastani B. Incidence and risk factors of transplant renal artery stenosis in living unrelated donor renal transplantation. J Ren Care 2010;36:149-52. 9. Pouria S, State OI, Wong W, Hendry BM. CMV infection is associated with transplant renal artery stenosis. QJM 1998;91:185-9. 10. Fauchald P, Vatne K, Paulsen D, Brodahl U, Sodal G, Holdaas H, et al. Long-term clinical results of percutaneous transluminal angioplasty in transplant renal artery stenosis. Nephrol Dial Transplant 1992;7:256-9. 11. Patel NH, Jindal RM, Wilkin T, Rose S, Johnson MS, Shah H, et al. Renal arterial stenosis in renal allografts: retrospective study of predisposing factors and outcome after percutaneous transluminal angioplasty. Radiology 2001;219:663-7.
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12. Halimi JM, Al-Najjar A, Buchler M, Birmele B, Tranquart F, Alison D, et al. Transplant renal artery stenosis: potential role of ischemia/ reperfusion injury and long-term outcome following angioplasty. J Urol 1999;161:28-32. 13. Rengel M, Gomes-Da-Silva G, Inchaustegui L, Lampreave JL, Robledo R, Echenagusia A, et al. Renal artery stenosis after kidney transplantation: diagnostic and therapeutic approach. Kidney Int 1998;68(Suppl):S99-106. 14. Sankari BR, Geisinger M, Zelch M, Brouhard B, Cunningham R, Novick AC. Post-transplant renal artery stenosis: impact of therapy on long-term kidney function and blood pressure control. J Urol 1996;155:1860-4. 15. Mammen NI, Chacko N, Ganesh G, Jacob CK, Shastry JC, Pandey AP. Aspects of hypertension in renal allograft recipients. A study of 1000 live renal transplants. Br J Urol 1993;71:256-8. 16. Siskind E, Lombardi P, Blum M, Tyrell R, Villa M, Kuncewitch M, et al. Significance of elevated transplant renal artery velocities in the postoperative renal transplant patient. Clin Transplant 2013;27: e157-60. 17. Merkus JW, Huysmans FT, Hoitsma AJ, Buskens FG, Skotnicki SH. Koene RA. Renal allograft artery stenosis: results of medical treatment and intervention. A retrospective analysis. Transpl Int 1993;6:111-5. 18. Chandrasoma P, Aberle AM. Anastomotic line renal artery stenosis after transplantation. J Urol 1986;135:1159-62. 19. Greenstein SM, Verstandig A, McLean GK, DaFoe DC, Burke DR, Meranze SG, et al. Percutaneous transluminal angioplasty: the procedure of choice for renal allograft artery stenosis. Transplant Proc 1987;19:2194-6.
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20. Matalon TA, Thompson MJ, Patel SK, Brunner MC, Merkel FK, Jensik SC. Percutaneous transluminal angioplasty for transplant renal artery stenosis. J Vasc Interv Radiol 1992;3:55-8. 21. Peregrin JH, Stribrna J, Lacha J, Skibova J. Long-term follow-up of renal transplant patients with renal artery stenosis treated by percutaneous angioplasty. Eur J Radiol 2008;66:512-8. 22. Beecroft JR, Rajan DK, Clark TW, Robinette M, Stavropoulos SW. Transplant renal artery stenosis: outcome after percutaneous intervention. J Vasc Interv Radiol 2004;15:1407-13. 23. Voiculescu A, Schmitz M, Hollenbeck M, Braasch S, Luther B, Sandmann W, et al. Management of arterial stenosis affecting kidney graft perfusion: a single-centre study in 53 patients. Am J Transplant 2005;5:1731-8. 24. Valpreda S, Messina M, Rabbia C. Stenting of transplant renal artery stenosis: outcome in a single center study. J Cardiovasc Surg (Torino) 2008;49:565-70. 25. Salvadori M, Di Maria L, Rosati A, Larti A, Piperno R, Becherelli P, et al. Efficacy and safety of Palmaz stent implantation in the treatment of renal artery stenosis in renal transplantation. Transplant Proc 2005;37:1047-8. 26. Geddes CC, McManus SK, Koteeswaran S, Baxter GM. Long-term outcome of transplant renal artery stenosis managed conservatively or by radiological intervention. Clin Transplant 2008;22:572-8. 27. Wong W, Fynn SP, Higgins RM, Walters H, Evans S, Deane C, et al. Transplant renal artery stenosis in 77 patientsedoes it have an immunological cause? Transplantation 1996;61:215-9. Submitted Jul 23, 2013; accepted Oct 10, 2013.