Renal Arterial Pseudoaneurysm After Partial Nephrectomy: Literature Review and Single-Center Analysis of Predictive Factors and Renal Functional Outcomes

Abstract

Introduction and Objective:

Partial nephrectomy (PN) represents the current surgical standard for T1 tumors. Renal arterial pseudoaneurysm is a rare but potentially life-threatening complication reported after PN. The aim of this study was to identify the factors associated with the occurrence of pseudoaneurysm after PN, specifically focusing on those requiring management with selective embolization. A literature review of the topic was performed.

Methods:

A retrospective review of the institutional PN database was performed from January 2011 to December 2016. Patients who underwent embolization for pseudoaneurysm represented a separated cohort to be compared with other patients (controls). Patients' and tumors' characteristics were considered. Univariable and multivariable analyses were used to test their eventual association with the occurrence of pseudoaneurysm.

Results:

A total of 1417 cases were evaluated. At a median of 21 days (interquartile range = 10–34), 20 patients (1.4%) developed postoperative pseudoaneurysm. The majority of patients (70%) presented with gross hematuria. The clinical suspicion was confirmed by contrast-enhanced computed tomography scan with angiography. Selective embolization was performed using endovascular coils. Technical success and clinical success rates were 100% and 95%, respectively. No difference was found in percentage estimated glomerular filtration rate (eGFR) preserved between patients who underwent embolization versus controls (median 82.6% versus 86.3%, P = .35). No differences in age, baseline renal function (as assessed by glomerular filtration rate [GFR]), tumor size, and R.E.N.A.L. were found between patients who reported and did not report pseudoaneurysm. In patients who developed pseudoaneurysm, longer operative time (225.6 minutes versus 193 minutes, P = .04), and cold ischemia time (48 minutes versus 29 minutes, P = .03) were reported.

Conclusion:

In our series, the occurrence of pseudoaneurysm was associated with longer operative and cold ischemia times. In patients who underwent selective embolization, renal function remained comparable with that of controls.

Introduction

Partial nephrectomy (PN) is an established surgical treatment for T1 renal masses.^1,2 This is because the nephron-sparing approach has showed similar oncologic outcomes and advantages in renal functional preservation when compared with radical nephrectomy.^3–5 However, it has been widely reported that PN increases the risk of iatrogenic vascular lesions, such as pseudoaneurysms and arteriovenous fistulas, due to the required renorrhaphy in a vascularized renal parenchyma.^6,7 These are rare but severe complications that can lead to hematuria, blood loss, and even hemorrhagic shock.^6,8

Particularly, renal arterial pseudoaneurysms may occur due to partial transection of arteries during tumor resection or renorrhaphy.⁹ The clinical presentation can vary depending on local pressure in aneurysm due to the blood flow and also on the effectiveness of the hemostasis. It can occur within the early postoperative period, but delayed presentation beyond 7 days after surgery is frequently observed as well.¹⁰ The typical clinical presentation is usually with acute bleeding episode, but patient's symptoms can vary from flank pain to acute shock.

The emergency transarterial embolization is an effective treatment modality for the management of hemodynamically unstable patients with renal arterial pseudoaneurysms.¹¹ It was reported to have minimal impact on renal function.^12–14

Current reports have associated centrally located tumors with a higher occurrence of pseudoaneurysm.³ Indeed, the complications developing after PN are theoretically considered to have a relationship with the tumor complexity, as assessed by standardized nephrometry scores.^15,16 Nevertheless, no studies found tumor complexity correlated with the occurrence of complications.¹² In summary, controversies still exist in the field. In this scenario, this study was set up. The primary aim was to look for predictive factors of the occurrence of pseudoaneurysm post-PN. The secondary aim was to evaluate the renal functional outcomes in patients undergoing embolization. A literature review of the topic accompanied the data analysis.

Patients and Methods

The institutional review board-approved PN database was reviewed to obtain data from consecutive patients who underwent PN for renal tumors from January 2011 to December 2016 (IRB 5065 and 15-1593).

Patients were divided into two groups based on whether receiving embolization for pseudoaneurysm or not. Patients who did not receive embolization represented the controls.

Patients' demographics and baseline characteristics (including age, race, gender, body mass index [BMI], American Society of Anesthesiologists [ASA] score, and Charlson Comorbidity Index [CCI]¹⁷), clinical tumor features (including tumor size and tumor R.E.N.A.L. nephrometry score¹⁸), and surgical variables (including surgical approach, operative time, blood losses, ischemia type and duration, and intraoperative complications, namely any injury to hollow viscus, pleural, ureteral, vascular, or surrounding organ) were collected and analyzed.

Specifically for the secondary aim of the study, renal functional data were extracted and analyzed: the preoperative estimated glomerular filtration rate (eGFR) was calculated by the Modification of Diet in Renal Disease (MDRD) equation. Eventual chronic kidney disease stage was defined as glomerular filtration rate (GFR) <60 mL/(minutes ·1.73 m²).¹⁹ At postoperative evaluation, eGFR preservation was calculated and defined as postoperative eGFR divided by baseline eGFR and expressed as percentage. The assessment of postoperative eGFR occurred between 6 and 12 months after PN. Patients were readmitted when reporting clinical symptoms, including bleeding with gross hematuria, abdominal pain, and hemorrhagic shock.

The eventual clinical suspicion of renal pseudoaneurysm was confirmed by contrast-enhanced computed tomography (CT) scan with angiography. Selective or super-selective embolization was performed using endovascular coils.

The technical success of the procedure was defined as the ability to successfully control any bleeding. The clinical success was defined as no patient's symptoms and no need for further management after embolization.

Patients were followed up with a clinical visit in 1 month after procedure and thereafter once every 6 months. Follow-up imaging was appointed as appropriate.

Statistical analysis

Continuous variables were described as means and standard deviations (SDs) or medians and interquartile ranges (IQRs), as appropriate. Categorical variables were described as frequencies and percentages. The nonparametric Mann–Whitney U-test and the χ² test were used for comparing the continuous and categorical variables between the groups. Univariable and multivariable analyses looked for eventual predictors of pseudoaneurysm deserving embolization. Statistical significance was set at P < .05. The analyses were performed by using SPSS v22 software (IBM SPSS Statistics, Armonk, NY; IBM Corp.).

Results

A total of 1417 patients underwent PN in our institution within the time span considered and were extracted. Twenty patients (1.4%) developed renal pseudoaneurysm, requiring embolization in the postoperative period and represented the studied cohort.

The remaining 1397 patients represented the controls.

The patients' and tumors' characteristics are reported in Table 1. When compared with controls, patients with pseudoaneurysm who underwent embolization were found comparable in age, BMI ASA score, CCI, clinical tumor size, and R.E.N.A.L. score (P > .05).

Table 1.

Patient and Tumor Characteristics

Variables	Embolization	Embolization	P
Variables	yes (n = 20)	no (n = 1397)	P
Age, years, (± SD)	59.6 (12.2)	62.3 (6.2)	.33
White race, n (%)	17 (85)	1193 (86.3)	.87
Male, n (%)	4 (20)	549 (39.3)	.08
BMI, med (IQR)	31 (26.4–36.5)	29.7 (26.1–34)	.48
ASA, med (IQR)	3 (2–3)	3 (3–3)	.58
CCI, med (IQR)	1 (0–2)	1 (0–2)	.12
Preop eGFR, med (IQR)	75.4 (55.2–88.5)	81.3 (63.8–96.5)	.20
Preop CKD, n (%)	5 (25)	271 (19.4)	.53
Tumor size on CT cm, med (IQR)	3.5 (2.7–4.6)	3.5 (2.5–4.7)	.58
R.E.N.A.L. score, med (IQR)	8 (7–9)	7 (6–9)	.10

ASA, American Society of Anesthesiologists; BMI, body mass index; CCI, Charlson Comorbidity Index; CKD, chronic kidney disease; CT, computed tomography; eGFR, estimated glomerular filtration rate; IQR, interquartile range; SD, standard deviation.

Median preoperative renal function as assessed by eGFR was comparable as well (75.4 [IQR 55.2–88.5] versus 81.3 [63.8–96.5] mL/(minutes ·1.73 m²), patients who underwent embolization versus controls, respectively, P = .20). Accordingly, the rate of patients who had preoperative chronic kidney disease was comparable between the groups (25.0% versus 19.4%, respectively).

As concerning the surgical variables (Table 2), the adoptions of the robotic versus the open approach and of the warm ischemia versus the cold ischemia were similar between the groups. When compared with controls, the patients who developed a pseudoaneurysm and underwent embolization had similar median blood losses (200 [150–350] versus 150 [150–300] mL, P = .27) and intraoperative complications, but were found with significantly increased mean operative time (225.6 minutes [SD 67.9] versus 193 minutes [SD 71.5], P = .04) and median cold ischemia time (48 minutes [IQR 40–60] versus 29 minutes [25–44], P = .03).

Table 2.

Surgical Outcomes and Functional Follow-Up Data

Variables	Embolization	Embolization	P
Variables	yes (n = 20)	no (n = 1397)	P
Approach
RPN, n (%)	12 (1.2)	998 (98.8)	.26
OPN, n (%)	8 (2)	399 (98)
Operation time, minutes, mean (± SD)	225.6 (67.9)	193 (71.5)	.04
Warm ischemia
n (%)	13 (65)	959 (70)
Time, minutes, med (IQR)	19.5 (13–28)	22 (17–28)	.2
Cold ischemia
n (%)	7 (35)	316 (23)	.03
Time, minutes, med (IQR)	48 (40–60)	29 (25–44)
Unclamped, n (%)	0 (0)	98 (7)
EBL, mL, med (IQR)	200 (150–350)	150 (100–300)	.27
Intraoperative transfusion, n (%)	1 (5)	53 (3.8)	.78
Time to embolization, days, med (IQR)	21 (10–36)
Follow-up times, months, median (IQR)	18 (8.9–38.2)	13.2 (4.4–27.5)	.14
Latest eGFR, mL/(minutes 1.73 m²), median (IQR)	62 (42.7–74.2)	70 (54.5–85.2)	.05
Latest follow-up %eGFR preservation, median (IQR)	82.6 (69.7–97.2)	86.3 (76.3–97.8)	.35

Numbers shown in bold denote values of statistical significance.

EBL, estimated blood loss; eGFR, estimated glomerular filtration rate; IQR, interquartile range; OPN, open partial nephrectomy; RPN, robotic partial nephrectomy; SD, standard deviation.

Univariable regression analyses confirmed operative time and cold ischemia time as the only statistically significant predictors of the occurrence of pseudoaneurysm worthy of management with embolization (P < .05).

As concerning the functional outcomes (Table 2), no difference in median percentage eGFR preserved was observed between patients who underwent embolization and the controls (82.6 [69.7–97.2] versus 86.3 [76.3–97.8], P = .35, respectively).

Subgroup analysis

The median time to readmission for the management of pseudoaneurysm was 21 days (IQR 10–34 days). Seventy-five percent of the cases presented within the first month after surgery. Table 3 gives in detail the patients' and the tumors' characteristics and the clinical presentation of all the analyzed pseudoaneurysm cases that required embolization. The majority (70%) presented to the clinician with gross hematuria, leading to initial diagnosis with contrast-enhanced CT. One case (5%) was incidentally discovered on follow-up CT scan. All the cases reported here who underwent embolization had confirmed pseudoaneurysm. In 1 case, the pseudoaneurysm was associated with an arteriovenous fistula.

Table 3.

Patient, Tumor, and Surgeon Characteristics and Clinical Presentation in Individual Patients

Patients no.	Gender	Age	R.E.N.A.L. score					Tumor size, cm	Procedure	Ischemia type/time, minutes		Tumor pathology	Clinical presentation and postoperative days
Patients no.	Gender	Age	R	E	N	A	L	Tumor size, cm	Procedure	Ischemia type/time, minutes		Tumor pathology	Clinical presentation and postoperative days
1	M	73	1	2	2	P	3	3.1	Robotic	Warm	13.0	Clear cell	None, routine follow-up, 276
2	F	62	1	2	1	P	2	3.0	Robotic	Warm	9.0	Clear cell	Abdominal pain, gross hematuria, 33
3	M	59	2	3	1	A	2	4.5	Robotic	Warm	29.0	Papillary	Hemorrhagic shock, 1
4	M	71	1	2	2	X	1	2.6	Robotic	Warm	20.0	Benign cyst	Gross hematuria, 10
5	M	60	1	2	3	A	2	3.5	Robotic	Warm	28.0	Clear cell	Gross hematuria, 10
6	F	67	1	2	2	A	3	1.6	Robotic	Warm	13.0	Papillary	Gross hematuria, 9
7	M	70	2	2	2	P	2	6.1	Robotic	Warm	19.5	Papillary	AKI, urosepsis, gross hematuria, 15
8	M	58	1	3	3	A	3	2.5	Robotic	Warm	13.5	Clear cell	Gross hematuria, 10
9	M	52	2	1	3	A	2	4.7	Robotic	Warm	18.1	Oncocytoma	Hypovolemia, gross hematuria, 31
10	M	64	1	2	1	A	3	2.3	Robotic	Warm	21.0	Clear cell	Urinary retention, gross hematuria, 37
11	F	76	1	3	3	P	1	3.1	Robotic	Warm		Papillary	Abdominal pain, 7
12	M	60	1	2	2	X	2	3.0	Robotic	Warm	32.0	Oncocytoma	Hemorrhagic shock, 1
13	M	60	3	2	3	X	3	7.3	Open	Cold	51.0	Papillary	Dizziness, oliguria, hypotension, 11
14	M	56	2	2	3	A	3	4.3	Open	Cold	44.0	Clear cell	Urinary retention, gross hematuria, 43
15	M	62	2	2	3	P	3	6.5	Open	Cold	60.0	Clear cell	Gross hematuria, clot retention 30
16	F	66	1	3	3	A	3	3.5	Open	Cold	24.0	Clear cell	Abdominal pain, 49
17	M	57	2	2	2	P	3	5.2	Open	Warm		Clear cell	Gross hematuria, 11
18	M	58	1	3	1	A	1	1.4	Open	Cold	48.0	Chromophobe	Gross hematuria, 30
19	M	58	2	1	1	X	2	4.2	Open	Cold	40.0	Clear cell	Bulge near incision, 391
20	M	65	2	2	2	P	3	4.3	Open	Cold	66.0	Papillary	Urinary sepsis, 27

AKI, acute kidney injury.

In the 95% of the cases, bleeding was successfully controlled during the first attempt angioembolization. Only 1 case required a further embolization due to the second bleeding episode 24 hours after the first episode.

No patients were lost at follow-up. No further bleeding episodes occurred within the 15 months of median follow-up.

Discussion

Literature data report an incidence of renal pseudoaneurysm equal to 0.5% and 1.7% after open and laparoscopic PN, respectively.^8,20,21 Anecdotal experiences are reported after robotic approach.²² One of the debated points is the timing of symptoms presentation when pseudoaneurysm occurs after PN. Cohenpour et al.²³ found a mean time to presentation of 12.2 days after surgery, and Netsch et al.^9,24 reported median time of presentation as 12.5 days postoperatively. In a review of 998 patients undergoing minimally invasive PN, 17 cases occurred with none presenting after 25 days postoperatively.²⁵

The common presenting complaints for such renal vascular lesions include gross hematuria, flank pain, and anemization.²¹ The different management approaches for patients who present with bleeding episode after PN include conservative, radiological, and surgical treatments. Conservative management with observation should be carefully selected only in small low-pressure pseudo aneurysms, as majority of these asymptomatic cases can recover spontaneously. Endovascular management is, however, preferred over watchful waiting especially in cases of large lesions that present with major bleeding episode. Surgical treatment, that is, radical nephrectomy, is second line deferred to only in nonresponsive cases.^23,24,26

It has been underlined by previous report that larger lesions, especially if misdiagnosed or untreated, can lead to progressive decline of renal function.²⁷ Conversely, Collins et al. tracked 41 postrenal arterial embolization patients for a median follow-up of 13.0 months and found that there were no significant changes in the GFR of the study population between the baseline and last available follow-up.¹⁴

In our series, the incidence of pseudoaneurysm was 1.2% for robotic and 2% for open PN cases, with no statistically significant difference in the incidence of pseudoaneurysm between the two groups. In our robotic series, the incidence of pseudoaneurysm was lower if comparable with that reported in the literature for conventional laparoscopic PN. The reasons of such advantage (thus minimal) could be the better visibility, dexterity, and superior parenchymal approximation allowed by robotics. Indeed, renorrhaphy has been described as an important aspect able to reduce the occurrence of pseudoaneurysm after PN.²⁸

Of note, 11 of our 20 pseudoaneurysm patients were placed on some sort of anticoagulant therapy postoperatively. Eight patients were on subcutaneous heparin (SQH), 1 patient had aspirin, whereas the remaining 2 cases were prescribed a combination of SQH and aspirin. Majority of these cases on anticoagulant presented early postsurgery but further study is needed to validate their influence on postoperative bleeding.²⁹

Pseudoaneurysm was diagnosed using contrast-enhanced CT scan or angiography. The average time period for presentation ranged from few hours postoperatively to a year after surgery in our study sample. All the cases in our study had undergone angiography with embolization. Technical success of angioembolization was 100% of our cases, whereas clinical success was 95% since 1 case required a second angioembolization due to recurrent bleeding. The success rates reported are similar to currently published studies.³⁰

Certain rare complications associated with embolization include arterial dissection, hypertension, and total loss of renal function. There was no postoperative renal infarction or loss of kidney function noted during follow-up. Our findings are in agreement with those presented in previous articles. Ghoneim et al. earlier reported good renal functional outcomes in their study group of 15 patients, except in 1 case with solitary kidney wherein renal functional decline was noted.³¹ All the cases in our study have functioning contralateral kidney. The percentage of eGFR preserved in study cases who underwent angioembolization is also similar to control group who did not require any endovascular treatment (82.6% versus 86.3%, P = .35).

On univariate analysis, we found operative time and cold ischemia times significantly associated with the need for embolization (P < .05). A possible explanation of the finding is that cold ischemia might be able to obscure bleeding vessels intraoperatively due to vascular spasm. Moreover, these parameters could be surrogates of the tumor complexity. Nevertheless, in our study, we found no correlation between R.E.N.A.L. score and incidence of vascular lesions. Nadu et al. reported higher pseudoaneurysm incidence in central tumors.³² Conversely, Chen et al. reported about 11 patients had renal arterial pseudoaneurysm and renal arteriovenous fistula after PN. The authors concluded that such complications may not have any relationship with the surgical procedure or the tumor complexity.¹² It is clear that further studies are needed to determine the effect of tumor complexity.

The major drawback of our study was the retrospective nature. Moreover, as the occurrence of renal pseudoaneurysms is low, we pooled the data from both open and robotic PN.

The unbalanced groups of patients who reported and did not report renal pseudoaneurysm amenable of embolization could have limited the statistical power on the analyses. Indeed, although having a large study population of 1417 patients, the small sample size and rare occurrence of pseudoaneurysm made it difficult to determine any factors with independent association with pseudoaneurysm.

Conclusion

We confirm that renal arterial embolization is a safe and effective method to treat postoperative bleeding episodes due to renal vascular lesions in patients stable enough to undergo embolization. Based on our experience, the occurrence of pseudoaneurysm was associated with longer operative and cold ischemia times. Selective angioembolization did not significantly worsen the renal function in comparison with the control group.

Footnotes

Disclosure Statement

J.H.K. certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the article (e.g., Employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patent filed, received or pending), are the following: Endocare, Inc., Intuitive.

J.S.C., MD, R.B., MD, O.K., MD, J.G., MD, P.M., MD, PhD, R.J.N., DO, and J.D., MD, have nothing to disclose.

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