Objectives: Endovascular therapy is the most common treatment for transplant renal artery stenosis; however, its long-term outcomes remain controversial, with no uniform standard for percutaneous transluminal angioplasty versus percutaneous transluminal stenting.
Materials and Methods: We retrospectively analyzed 26 patients with transplant renal artery stenosis who underwent endovascular therapy. We evaluated long-term efficacy of endovascular therapy and the reasonable choice of treatment.
Results: Serum creatinine increased significantly at onset of transplant renal artery stenosis (113.88 ± 37.573 before vs 279.31 ± 94.98 μmol/L during stenosis; P₁ < .001), and endovascular therapy had a good short-term effect (279.31 ± 94.98 during stenosis vs 139.54 ± 124.40 μmol/L at 2 weeks posttreatment; P₂ = .002). Long-term efficacy of endovascular therapy was stable (139.54 ± 124.40 at 2 weeks posttreatment vs 150.69 ± 180.72 at 6 months vs 161.58 ± 174.49 μmol/L at last follow-up; P₃ > .05). Blood pressure increased significantly at onset of transplant renal artery stenosis (126.65 ± 16.11 before vs 159.62 ± 25.84 mm Hg during stenosis; P₁ < .001). Moreover, the short-term effect of endovascular therapy was good (159.62 ± 25.84 during stenosis vs 128.73 ± 14.22 mm Hg at 2 weeks posttreatment; P₂ < .001). Long-term effects remained stable (128.73 ± 14.22 at 2 weeks posttreatment vs 131.15 ± 14.55 at 6 months vs 138.50 ± 16.82 mm Hg at last follow-up; P₃ > .05). Peak systolic velocity decreased significantly after endovascular therapy (176.6 ± 67.93 during stenosis vs 114.24 ± 67.93 cm/s at 2 weeks posttreatment; P < .001).
Conclusions: Endovascular therapy is effective in transplant renal artery stenosis treatment and has a low incidence of complications. Percutaneous transluminal angioplasty should be performed routinely during endovascular therapy. After dilation, if stenosis remains >25% or retracted, then percutaneous transluminal stenting is recommended. Otherwise, percutaneous transluminal angioplasty is preferred.

Key words : Endovascular therapy, End-stage renal disease, Kidney transplantation, Percutaneous transluminal angioplasty, Percutaneous transluminal stenting

Introduction

Compared with dialysis, kidney transplant has obvious advantages to prolong the survival and improve the quality of life of patients with end-stage renal disease; however, factors such as rejection, infection, and surgical complications may affect the long-term survival of patients with transplanted kidney.^1,2 Transplant renal artery stenosis (TRAS) contributes to 75% of all vascular complications and has an incidence of 1% to 23%, typically between 3 months and 2 years after a kidney transplant. Although the incidence is not very high, severe TRAS can be accompanied by renal artery thrombosis and graft loss.^3-5 The classic triad of symptoms in TRAS includes worsening renal function, refractory hypertension, and fluid retention; TRAS should be suspected when a patient presents with these symptoms. Of course, rejection, infection, urinary tract obstruction, and other diseases should be excluded.^6,7 Several factors may increase the risk for TRAS, including injury to the vascular endothelium during organ acquisition and transplant, the use of incorrect surgical suture techniques, a prolonged cold ischemic time, ischemia-reperfusion injury, graft rejection, and cytomegalovirus infection.^8-10 The effects of TRAS on a transplanted kidney are reversible; thus, early recognition and appropriate intervention are crucial.

Endovascular therapy (EVT) is the most com-monly used treatment for TRAS. Although many studies have confirmed the short-term and medium-term efficacy of EVT, its long-term efficacy remains controversial, and there are no uniform criteria for the selection of percutaneous transluminal angioplasty (PTA) or percutaneous transluminal stenting (PTS). Therefore, in this study, we retrospectively evaluated patients with TRAS who underwent EVT at the Second Affiliated Hospital of Nanhua University, and we evaluated the long-term efficacy and safety of EVT and the choice of the EVT mode.

Materials and Methods

Ethics statement
This study was conducted according to the principles of the Declaration of Helsinki and was approved by the Ethics Committee of the Second Affiliated Hospital of Nanhua University. All participants provided written informed consent prior to enrollment.

Demographic and clinical characteristics
We retrospectively analyzed 26 patients (mean patient age, 49.9 ± 9.3 years; 15 men and 11 women) with TRAS who underwent EVT at the Second Affiliated Hospital of Nanhua University from January 2010 to December 2021. Data were collected from the hospital’s electronic medical records, including age, sex, body mass index, primary diseases causing renal failure, number of human leukocyte antigen mismatches, recipient complications, donor characteristics, cold ischemic time, arterial anasto-mosis patterns, clinical signs and symptoms of TRAS, onset time of TRAS, stenosis site, EVT pattern, TRAS-related complications, and changes in serum creatinine level. The peak systolic velocity (PSV) of the transplanted renal artery and changes in blood pressure were studied in patients with TRAS who underwent EVT.

The kidney transplant was performed by experienced physicians from the same medical team using standard procedures; basiliximab or rabbit antithymocyte globulin was routinely used for immune induction. The postoperative immunosup-pressive program was as follows: methylprednisolone was administered (500 mg during the operation; 500 mg on day 1 after the operation; oral consumption and slow reduction in the dose from day 2, with the dose maintained at 5 mg at 2 weeks after the operation); the target trough concentration of tacrolimus was maintained at 5 to 9 ng/mL; and the area under the curve value for mycophenolate concentration was maintained at 30 to 60 mg·h/L. Antibiotics were routinely used to prevent infection after the operation; moreover, sulfamethoxazole was used to prevent pneumocystis, whereas ganciclovir was used to prevent cytomegalovirus infection, based on conditions and wishes expressed by the patients.

Delayed graft function was defined as a kidney injury that required dialysis in the first week after kidney transplant.¹¹ The diagnostic criteria for diabetes were consistent with the diagnostic criteria of the American Diabetes Association¹² except that an oral glucose tolerance test was not performed. Refractory hypertension was defined as hypertension that could be controlled with 3 or more classes of antihypertensive drugs.¹³ Deterioration of renal function was defined as an increase of 20% in the serum creatinine level.¹⁴

Diagnosis of transplant renal artery stenosis
Transplant renal artery stenosis should be suspected when a patient presents with 1 of the following symptoms: (1) sudden onset of refractory hyper-tension, (2) unexplained worsening of renal function, and (3) unexplained fluid retention. First, we performed Doppler ultrasonography and considered the following indicators as criteria for TRAS screening: PSV >200 cm/s, interlobar arterial resistance index <0.7 to 0.5, and acceleration time <0.06 to 0.15 s.15 The patients suspected of having TRAS by Doppler ultrasonography were subjected to computed tomography angiography (CTA) (Figure 1, A and B) or enhanced magnetic resonance angiography (MRA) to confirm the diagnosis. The final diagnosis was made using invasive digital subtraction angiography (DSA) if the noninvasive tests did not allow for a definitive diagnosis or if EVT was required by the patients. The degree of stenosis was classified according to the canal diameter stenosis proportion: mild (stenosis from 25% to 50%), moderate (stenosis between 50% and 75%), and severe (stenosis ≥75%).¹⁶

Treatment program for transplant renal artery stenosis
According to the European Association of Urology (EAU) guidelines on renal transplantation,17 patients with mild stenosis should be treated conservatively if their renal transplant function is stable, provided there is no obvious change in their hemodynamics, the renal blood flow is abundant, their blood pressure can be effectively controlled, and there is no obvious fluid retention. For patients with moderate to severe stenosis, EVT (including PTA or PTS) is the first treatment choice, especially in cases of uncontrolled hypertension, renal graft function deterioration, or stenosis progression. In this study, EVT was performed by experienced interventional radiologists and vascular surgeons. The patients were given local anesthesia, and a puncture was made in the ipsilateral or contralateral common femoral artery under ultrasonographic guidance. Nonselective iliac arteriography was performed to confirm the stenotic lesion. A guidewire was used to insert a 5F sheath into the transplanted renal artery. Selective angiography was performed to measure the stenotic lesion. Appropriate saccules were selected for PTA (Figure 2, A-C). A stent was placed if the stenosis remained at >25% or retracted after dilation (Figure 2, D-F); otherwise, only PTA was performed. The anticoagu-lation program was as follows: (1) intraoperative heparinization was performed; (2) subcutaneous injection of low-molecular-weight heparin was administered within 3 days after the operation; (3) oral clopidogrel was administered for 1 month to patients who underwent only PTA; and (4) oral aspirin and clopidogrel were prescribed for 6 months to patients with stent implants. The criteria for successful EVT included stenosis <25% and restoration of renal blood flow after the intervention (Figure 1, C and D).

Perioperative treatment and postoperative follow-up
The blood pressure levels, serum creatinine levels, and color Doppler ultrasonographic images of the transplanted kidneys were monitored during the perioperative period, and surgery-related complica-tions were recorded, including hemorrhage, pseudoaneurysms, arterial dissection, and infection. The patients were followed up regularly at the outpatient department after the operation, and antirejection drugs were administered to them regularly. If necessary, the transplanted kidney was checked with Doppler ultrasonography.

Statistical analyses
All data were analyzed with SPSS software (version 28). The measurement data are expressed as mean values ± SD (normally distributed data) or median values (variables that were not normally distributed), and the enumeration data are expressed as frequency and percentages. The paired t test was used to compare the PSV before and after the operation, whereas the independent sample t test was used to compare the efficacy of PTA and PTS. Analysis of variance was used to analyze the serum creatinine levels and blood pressure levels before and after the operation. P < .05 was considered statistically significant.

Results

Clinical features
The clinical and demographic characteristics of the patients are presented in Table 1. The most common primary diseases causing renal failure were chronic glomerulonephritis in 10 patients (38.5%), diabetic nephropathy in 5 patients (19.2%), hypertensive nephropathy in 3 patients (11.5%), polycystic kidney disease in 1 patient (3.8%), and other unclassified diseases in 7 patients (26.9%). Six (23.1%) patients had diabetes mellitus, 18 (69.2%) had hypertension, and 9 (34.6%) had aortoiliac atherosclerosis. The donor characteristics were as follows: 9 donors (34.6%) were >50 years old, 23 (88.5%) were brain death donors, 2 (7.7%) were cardiac death donors, and 1 (3.8%) was a living related donor. The mean number of mismatches was 2.4 (2.4 ± 0.8), and the mean cold ischemic time was 104 minutes (104 ± 24.4). The renal artery was anastomosed with the internal iliac artery in 22 (84.6%) patients and with the external iliac artery in 4 (15.4%) patients. The mean time until TRAS onset was 12 months (range, 3 days to 30 months). The clinical manifestations of TRAS included renal function deterioration in 24 (92.3%) patients, refractory hypertension in 9 (34.6%) patients, pulmonary edema in 2 (7.7%) patients, and delayed graft function in 1 (3.8%) patient. Arterial stenosis was located around the anastomosis in 19 cases (73.1%), distal anastomosis in 5 cases (19.2%), and other locations in 2 cases (7.7%).

Effect of endovascular therapy treatment
A total of 26 patients underwent EVT and were followed up for 41 months (range, 8-125 months) on average. One patient died of a cerebrovascular accident 2 years after EVT. Successful PTA was performed in 12 (46.2%) patients. Percutaneous transluminal stenting was performed in 13 (50%) patients; in one of those cases, the stent failed to pass through the narrow segment, and regular hemodialysis was performed after treatment failure. In another one of those cases, the patient relapsed 3 months after PTA and then underwent PTS again; after 12 months of follow-up, the creatinine level was normal. One other patient relapsed 2 months after PTA and then underwent PTS, and after 125 months of follow-up, the vascular stent was unobstructed and the creatinine level increased to 288 μmol/L. One patient relapsed 12 months after PTS and underwent PTA with stent, and after 34 months of follow-up, the creatinine levels were normal. The success rate of early treatment was 96.2% (25/26), the one-time success rate was 84.6% (22/26), and the overall success rate was 96.2% (25/26). Two patients presented with arterial dissection and were treated with covered stents and cured; 1 patient presented with an aneurysm and was treated with surgery and cured; no other complications such as significant bleeding and infection were observed (Table 2).

The serum creatinine level increased significantly upon the onset of TRAS (113.88 ± 37.573 before TRAS vs 279.31 ± 94.98 μmol/L during TRAS; P1 < .001). The EVT had a good short-term effect (279.31 ± 94.98 during TRAS vs 139.54 ± 124.40 μmol/L at 2 weeks after treatment; P₂ = .002) and a stable long-term effect (139.54 ± 124.40 at 2 weeks after treatment vs 150.69 ± 180.72 at 6 months after treatment vs 161.58 ± 174.49 μmol/L at the last follow-up; P₃ > .05), as shown in Figure 3. The blood pressure levels increased significantly upon the onset of TRAS (126.65 ± 16.11 before TRAS vs 159.62 ± 25.84 mm Hg during TRAS; P₁ < .001). Endovascular therapy had a good short-term effect (159.62 ± 25.84 during TRAS vs 128.73 ± 14.22 mm Hg at 2 weeks after treatment; P₂ < .001) and a stable long-term effect (128.73 ± 14.22 at 2 weeks after treatment vs 131.15 ± 14.55 at 6 months after treatment vs 138.50 ± 16.82 mm Hg at the last follow-up; P3 > .05), as shown in Figure 4. The PSV decreased significantly after EVT (176.60 ± 67.93 during TRAS vs 114.24 ± 67.93 cm/s at 2 weeks after treatment; P < .001), as shown in Figure 5.

At the same time, we compared the change values (Δ) in the serum creatinine levels, systolic blood pressure levels, and PSV between PTA and PTS. We found 3 changes in the serum creatinine levels in the patients who underwent PTA and PTS (Δ1, from during TRAS to 2 weeks after treatment; Δ2, from during TRAS to 6 months after treatment; Δ3, from the period during TRAS until the last follow-up), and these changes were not significantly different from each other (P₁ = 0.527, P₂ = 0.560, and P₃ = 0.358, respectively). Three systolic blood pressure variation values (Δ1, Δ2, and Δ3) were not significantly different from each other (P₁ = 0.421, P₂ = 0.378, and P₃ = 0.862, respectively). There was no significant difference (P = .909) in one change values of PSV (Δ1, from during TRAS to 2 weeks after treatment) between the patients who underwent PTA and PTS (Table 3).

Discussion

Transplant renal artery stenosis generally occurs between 3 months and 2 years after kidney transplant, but this is not absolute. In our study, 1 patient was diagnosed 3 days after the operation. The patient had a low urine output and high creatinine level on postoperative day 2. Doppler ultrasonography of the transplanted kidney indicated renal blood flow dilution, a low resistance index, and a PSV of 220 cm/s, suggesting renal artery stenosis. After the possibility of rejection and urinary tract obstruction were excluded, TRAS was initially considered, and finally a CTA was performed to identify TRAS. On postoperative day 4, PTS was performed under local anesthesia. The urine volume increased significantly and the creatinine level decreased after the operation. The patient prognosis was good. We believed that the occurrence of TRAS in the perioperative period was mostly related to the surgical anastomosis technique, renal artery torsion, and mechanical compression.

In our case, we considered anastomotic stenosis caused by transplanted renal artery torsion. This conclusion was based on the following observations: (1) during the operation, the transplanted kidney was well filled, ruddy in color, and plump in texture, and the urine was discharged from the ureter 2 minutes after the blood flow was restored; (2) the urine volume was more than 4000 mL/d over the first 2 days after the operation, but the urine volume decreased on day 3 after ambulation; and (3) the CTA and DSA showed that the anastomotic stoma was angulated and that the angle was larger than that during the operation. The following lessons were learned: (1) during the operation, the transplanted kidney should be fixed properly in the iliac fossa, and the stability of the transplanted kidney and the anastomosis angle should be observed; (2) the position of the transplanted kidney and the anastomosis angle should be checked again before closing the abdominal wall wound; (3) sudden and strenuous activities should be avoided by the patient in the early postoperative period; and (4) the possibility of TRAS should also be considered in the early reduction of urine volume. Ayvazoglu and colleagues and Aktas and colleagues reported 16 and 14 cases of tortuosity of the renal artery or renal vein, respectively, but these cases had immediate surgical intervention with good recovery after realignment of the location of the transplanted kidney.^18,19

The classic triad of symptoms of TRAS involves worsening graft function, refractory hypertension, and fluid retention.⁷ In our study, the most common presentation was worsening graft function in 24 (92.3%) patients, followed by refractory hypertension in 9 (34.6%) patients and pulmonary edema in 2 (7.7%) patients. Episodic pulmonary edema, which is accompanied by normal cardiac function and is known as Pickering syndrome, is a rare clinical presentation in patients with TRAS.²⁰ The clinical manifestations of TRAS in our study were similar to those reported in most other studies.^15,20,21

In our study, although most of the patients presented with more than 2 symptoms, 2 patients presented with pure refractory hypertension and during outpatient follow-up when the blood pressure was found to be suddenly difficult to control, warranting vigilance for TRAS. Interestingly, 1 additional patient in our study was diagnosed with TRAS after worsening renal function while being administered benazepril. Benazepril belongs to a class of angiotensin-converting enzyme inhibitors (ACEIs); it is noteworthy that ACEIs and angiotensin II receptor antagonists (ARBs) are contraindicated in patients with bilateral renal artery stenosis because, although ACEIs and ARBs can dilate the entry and exit arterioles simultaneously, these have a greater effect on the exit arterioles than on the entry arterioles. Therefore, after administration of ACEIs or ARBs, the blood flowing through the glomerulus would flow out faster, the pressure inside the glomerular capsule would decrease, and the filtration pressure would also decrease, leading to the reduction of glomerular filtration. The ACEIs and ARBs have been reported to have the same effects on patients with bilateral renal artery stenosis.^22,23

There is a standardized procedure for the diagnosis of TRAS at our center. Doppler ultrasonog-raphy is the preferred imaging technique for early screening and follow-up of TRAS, and PSV of the renal artery anastomosis is the basic diagnostic parameter once suspicious symptoms are first observed on the Doppler ultrasonography results. However, the diagnosis of TRAS must be combined with other indexes such as resistive index, PSV of the interlobar arteries, and blood flow richness assessments. In our study, the PSV was >200 cm/s in <50% of the patients (12 patients, 46.2%). Regarding the reference thresholds in terms of the ultraso-nographic diagnostic definition of TRAS, a wide variation was noted, with the PSV ranging from 180 to 400 cm/s,^13,24,25 resistive index being <0.7 to 0.523,²⁵ and the acceleration time being >0.06 to 0.15 s.²⁶

The EAU guidelines¹⁷ state that Doppler ultraso-nography is the accepted primary method for TRAS diagnosis and is widely used in screening and follow-up. Although it is highly operator-dependent, the results of Doppler ultrasonography are nevertheless strongly suggestive of the presence of TRAS when the PSV is >2.0 m/s, with a specificity of 60% to 98%. After initial diagnosis by Doppler ultrasonography, a CTA or MRA should be mandatorily performed; MRA reduces the impact of the contrast medium on the kidneys. However, MRA tends to overestimate the severity of the stenosis, limiting its routine use. Patients indeterminate on noninvasive testing or those who require EVT should undergo a final diagnosis using invasive DSA. In addition, we used carbon dioxide-DSA during EVT, which is particularly suitable for patients with severe renal impairment, to avoid contrast-induced nephrotoxicity. Studies have shown that carbon dioxide is a safe, inexpensive, and widely used intravascular contrast agent that, because of its characteristics, is expected to become the first-choice contrast agent for patients with renal impairment or severe contrast allergy.²⁷

Many studies have shown that the anastomosis is the most common site for TRAS stenosis (incidence, 25%-78%).^28,29 However, proximal anastomosis TRAS may also occur, with an incidence of 6% to 10%14,30 (11%-59% after anastomosis).^31,32 The diffuse stenosis ranges from 6% to 20%.^28,33 In our study, peri-anastomotic stenosis was the most common site of stenosis in 19 (73.1%) patients, followed by distal anastomosis in 5 (19.2%) patients and other site in 2 (7.7%) patients. The occurrence of TRAS is related to factors such as expanded criteria donor, athe-rosclerosis, prolonged cold ischemic time, surgical technique, delayed renal graft function recovery, rejection, cytomegalovirus infection, calcineurin inhibitor usage, and mechanical compression.

The relationship between TRAS and neonatal class II antibodies deserves more attention, and it has been suggested that patients with neonatal class II antibodies should be screened for TRAS.³⁴ The EAU guidelines¹⁷ suggest that TRAS with stenosis of >50% and clinical manifestations should be treated actively; however, the indications and methods for treatment remain controversial. The preferred treatment for TRAS is EVT, including PTA and PTS. Pini and colleagues conducted a meta-analysis of 30 studies and evaluated the technical success rate of both PTA and PTS. The average technical success rate was 95.3%, ranging from 73% to 100% (95% CI, 92.7%-97.9%; P = .001).¹⁵ In our study, in 1 patient, the stent failed to pass through the stenosis with a guidewire, and 3 other patients underwent secondary EVT, with an early treatment success rate of 96.2% (25/26) and a one-time success rate of 84.6% (22/26). More importantly, we also conducted a long-term follow-up of the included patients; the average follow-up duration was 41 months (8-125 months). The overall success rate of 96.2% (25/26) confirmed that the long-term efficacy of EVT was satisfactory.

The choice between PTA and PTS in EVT remains controversial. It appears that PTS may have a more reliable effect than PTA; however, PTS is expensive, requires long-term anticoagulation therapy, and is accompanied by stent-related complications. In our opinion, EVT should first be performed with routine PTA alone; if the stenosis remains at >25% after dilation or if there is retraction after dilation, PTS should be performed. Our results showed no significant difference between PTA and PTS with regard to the short-term, medium-term, and long-term efficacy. However, 2 observations were made. First, patients’ wishes should be a priority during EVT. For example, individual patients could choose not to follow our recommendations. Because this was a retrospective study, we could not collect any data in this regard. Patients who chose PTA relapsed at first and were treated again with PTA; however, 1 patient who chose PTS relapsed at first and was treated with balloon dilatation again.

Pini and colleagues¹⁵ also analyzed the related complications, the incidence of which ranged from 0% to 25%. In the 1119 patients included in that study, 101 (9%) complications were recorded, including 36 (3.2%) puncture site hematomas or pseudoaneurysms, 20 (1.8%) renal artery or renal artery branch dissections, 11 (1.0%) stent dislocations or displacements, 9 (0.8%) stent occlusions or renal artery thromboses, 8 (0.7%) contrast agent-induced nephrotoxicity cases, 6 (0.5%) allograft losses (1 caused by iodized contrast-agent toxicity), 3 (0.3%) renal or iliac artery ruptures, 2 (0.2%) massive hemorrhages, 2 (0.2%) segmental renal infarctions, 1 (0.1%) scrotal hematoma, 1 (0.1%) peripheral branch occlusion, and 1 (0.1%) polar renal artery occlusion.¹⁵ In our present study, 3 (11.5%) patients had complications; 2 renal artery dissections were cured with covered stents, and 1 pseudoaneurysm was cured with surgery.

The retrospective and nonrandomized design is the main limitation of our study, and the relatively small sample size would require a large prospective trial to confirm our results. In addition, we did not compare the etiology of TRAS, nor did we routinely perform CTA or MRA in the patients after EVT.

Conclusions

Our study showed that EVT is not only effective in the treatment of TRAS in the early stages but is also satisfactory in the medium and long terms, with a low incidence of complications. The choice of PTA or PTS in EVT has been controversial. We recommend that routine PTA should be performed first during EVT. If the stenosis remains >25% after dilation or if the stenosis is retracted after dilation, PTS should be performed. Otherwise, PTA alone should be performed.

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