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Patient factors associated with 30-day complications after partial nephrectomy: A contemporary update
Urologic Oncology: Seminars and Original Investigations ] (2016) ∎∎∎–∎∎∎
Original article
Patient factors associated with 30-day complications after partial nephrectomy: A contemporary update Harras B. Zaid, M.D.a, William P. Parker, M.D.a, Christine M. Lohse, M.S.b, John C. Cheville, M.D.c, Stephen A. Boorjian, M.D.a, Bradley C. Leibovich, M.D.a, R. Houston Thompson, M.D.a,* b
a Department of Urology, Mayo Clinic and Mayo Medical School, Rochester, MN Department of Health Sciences Research, Mayo Clinic and Mayo Medical School, Rochester, MN c Department of Pathology, Mayo Clinic and Mayo Medical School, Rochester, MN
Received 5 July 2016; received in revised form 20 October 2016; accepted 4 November 2016
Abstract Introduction: Patient-level factors associated with perioperative complications after partial nephrectomy (PN) have not been well described in a contemporary series. Methods: Single-institution retrospective study evaluating patients undergoing open, laparoscopic, and robotic PN between 2001 and 2012. Univariable and multivariable logistic regression models were evaluated to assess factors associated with complications within 30 days of surgery. Results: We identified 1,763 patients who underwent 1,773 PNs between 2001 and 2012. From 2001 to 2006, 766 PNs were performed (85% open, 15% laparoscopic, and o1% robotic); in contrast, from 2007 to 2012, 1,007 PNs were performed (75% open, 8% laparoscopic, and 17% robotic); P o 0.001. Overall, 241 (14%) PNs resulted in an early surgical complication. Patients undergoing a minimally invasive approach had smaller tumors (P o 0.001), were less likely to have a solitary kidney (P o 0.001), and had a lower Charlson score (P ¼ 0.004). On multivariable analysis, factors independently associated with an increased risk of any complication included male sex (odds ratio [OR] ¼ 1.40), solitary kidney (OR ¼ 1.71), estimated glomerular filtration rate (OR ¼ 2.89 for estimated glomerular filtration rate o30), Charlson score (OR ¼ 1.97 for Charlson score Z3), and tumor size (OR ¼ 1.12 for each 1-cm increase in tumor size); meanwhile, laparoscopic and robotic approaches were associated with a lower risk for complication (OR ¼ 0.017 and 0.016, respectively), all P o 0.05. Conclusion: Several patient-level factors are associated with 30-day complications after PN, regardless of surgical approach. These data may inform counseling before PN, including potential identification and selection of high-risk surgical candidates for percutaneous ablative approaches. r 2016 Elsevier Inc. All rights reserved.
Keywords: Complication; Laparoscopic; Partial nephrectomy; Percutaneous ablation; Robotic; Outcomes
1. Introduction Radical nephrectomy has historically been the treatment of choice for localized renal cell carcinoma. However, nephron-sparing surgery including open partial nephrectomy (OPN), laparoscopic partial nephrectomy (LPN), and robotic partial nephrectomy (RPN) are now favored for the management of T1 masses. Indeed, American Urological Association (AUA) and European Association of Urology Corresponding author. Tel.: þ1-507-266-9968; fax: þ1-507-284-4951. E-mail address: [email protected] (R.H. Thompson). *
http://dx.doi.org/10.1016/j.urolonc.2016.11.001 1078-1439/r 2016 Elsevier Inc. All rights reserved.
(EAU) guidelines encourage nephron preservation when technically feasible [1,2]. These recommendations are based partly on mounting evidence that partial nephrectomy (PN), compared with radical nephrectomy, may decrease the risk of chronic kidney disease [3]. Although PN still remains the treatment of choice in healthier patients [2], percutaneous ablation and surveillance may be selected in certain patients with competing comorbidities [4]. However, PN is often technically more challenging than radical nephrectomy and remains underused in the community despite perceived benefits [5,6]. Over the past 2 decades, practice patterns have also changed, with
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progressive shift from OPN to minimally invasive approaches [7]. The advent of robotics, furthermore, has augmented laparoscopy to make minimally invasive PN more technically accessible to practicing urologists [8]. As treatment patterns continue to change, comprehensive comparative data comparing OPN with minimally invasive PN are lacking [9]. Furthermore, although minimally invasive approaches have been demonstrated to be safe [7], few studies have documented patient-level risk factors influencing outcomes in those undergoing PN, adjusting for surgical approach. Indeed, a better understanding of these risk factors could potentially inform preoperative counseling and help identify patients who may be candidates for surveillance or percutaneous ablative approaches. Herein, we describe our institutional experience with PN from 2001 to 2012, a contemporary cohort, to comprehensively evaluate patient-level factors associated with 30-day perioperative morbidity. 2. Patients and methods
surgical procedure, and pneumothorax. Pathologic features included tumor size and histologic subtype (renal cell carcinoma or benign). 2.3. Statistical methods Continuous features were summarized with medians and interquartile ranges; categorical features were summarized with frequency counts and percentages. We compared features between an early cohort (2001–2006) and a later cohort (2007–2012) to assess temporal trends in practice patterns using Wilcoxon rank-sum, chi-square, and Fisher exact tests, where appropriate. Associations with any early surgical complication were evaluated using logistic regression models and summarized with odds ratios (ORs) and 95% CIs. A multivariable model was developed using stepwise selection with the P value for a feature to enter or leave the model set to 0.05. Statistical analyses were performed using version 9.3 of the SAS software package (SAS Institute, Cary, NC). All tests were two-sided and P o 0.05 were considered statistically significant.
2.1. Patient selection
3. Results
After institutional review board approval, we queried the Mayo Clinic Nephrectomy Registry to identify 1,763 patients who underwent 1,773 PNs for solid renal masses between 2001 and 2012. Patients with bilateral synchronous disease, von Hippel-Lindau syndrome, or tuberous sclerosis syndrome, were excluded.
A comparison of clinical, surgical, and pathologic features by year of surgery (2001–2006 vs. 2007–2012) is shown in Table 1. As can be seen, patients undergoing PN between 2007 and 2012 tended to be younger with higher eGFRs, have lower Charlson and ECOG scores, and present less frequently with tumors in a solitary kidney (all P o 0.05). Between 2001 and 2006, 766 PNs were performed (85% open, 15% laparoscopic, and o1% robotic); in contrast, between 2007 and 2012, 1,007 PNs were performed (75% open, 8% laparoscopic, and 17% robotic); P o 0.001. When compared with OPN, patients undergoing a minimally invasive approach had smaller tumors (2.2 vs. 3.2 cm; P o 0.001), were less likely to have a solitary kidney (3% vs. 9%; P o 0.001), and had lower Charlson scores (0 vs. 1; P ¼ 0.004). A full list of early complications is included in Table 2. No patient died intraoperatively. There were 241 (14%) PNs that resulted in an early surgical complication, with a similar rate regardless of period (P ¼ 0.94). Overall, 119 (7%) PNs experienced a Clavien grade 3, 4, or 5 complication, which was similar between 2001–2006 and 2007– 2012 (6% vs. 7%, P ¼ 0.38). With the exception of hemorrhage (2% vs. 5%; P ¼ 0.009) and wound infection or dehiscence (3% vs. 1%, P ¼ 0.044), other complications were similar between 2001–2006 and 2007–2012. To better evaluate these bleeding complications, hemorrhage events were stratified by surgical approach and were similar between OPN (n ¼ 54, 4%) and minimally invasive PN (n ¼ 11, 3%), P ¼ 0.48. Furthermore, wound dehiscence occurred only in
2.2. Clinical, surgical, and pathologic features Clinical features included year of surgery, age at surgery, sex, estimated glomerular filtration rate (eGFR) at diagnosis calculated using the Chronic Kidney Disease Epidemiology Collaboration formula, Eastern Cooperative Oncology Group (ECOG) performance status at surgery, Charlson score at surgery, and obesity (defined as body mass index Z30). Surgical features included approach to PN (open— OPN, laparoscopic—LPN, or robotic—RPN), surgical margin status, estimated blood loss, transfusion rates, length of hospital stay, and complications within 30 days of surgery including death, hemorrhage (defined as bleeding resulting in an intervention such as reoperation or angioembolization, or a hematoma confirmed on imaging), deep vein thrombosis, pulmonary embolism, myocardial infarction, wound infection or dehiscence (defined as infection requiring antibiotics or drainage, or a separation of the layers of the surgical wound requiring intervention), abscess (defined as abscess requiring antibiotics or drainage), urine leak, sepsis (defined as bacteremia that resulted in hypotension or admission to the intensive care unit), acute renal failure, loss of kidney, need for an additional
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Table 1 Comparison of baseline features by year of surgery. Sample sizes for features with missing data are indicated in italics in parentheses Feature
Age at surgery, y eGFR, mL/min/1.73 m2; (N ¼ 1,741) Charlson score (N ¼ 1,768) Tumor size, cm; (N ¼ 1,750) Sex Female Male Solitary kidney ECOG performance status (N ¼ 1,769) 0 Z1 Type of PN Open Laparoscopic Robotic-assisted laparoscopic Histologic subtype Benign RCC Obese (N ¼ 1,734)
All N ¼ 1,773
2001–2006 N ¼ 766 Median (IQR)
2007–2012 N ¼ 1,007
P value
60 79 0 3.0
o0.001 o0.001 o0.001 0.080
661 (37) 1,112 (63) 136 (8)
62 (53–71) 64 (51–75) 1 (0–2) 3.0 (2.0–4.2) N (%) 275 (36) 491 (64) 76 (10)
386 (38) 621 (62) 60 (6)
0.29
1,632 (92) 137 (8)
692 (90) 73 (10)
940 (94) 64 (6)
0.014
1,407 (79) 196 (11) 170 (10)
649 (85) 115 (15) 2 (o1)
758 (75) 81 (8) 168 (17)
o0.001
355 (20) 1,418 (80) 752 (43)
147 (19) 619 (81) 291 (40)
208 (21) 799 (79) 461 (46)
0.45
61 72 1 3.0
(52–68) (58–86) (0–2) (2.0–4.3)
(51–67) (66–93) (0–2) (2.1–4.4)
0.002
0.009
ECOG ¼ Eastern Cooperative Oncology Group; IQR ¼ interquartile range; RCC ¼ renal cell carcinoma.
patients undergoing OPN (n ¼ 33, 2%), with no such events in patients undergoing minimally invasive PN (P o 0.001). Median blood loss was significantly lower in patients undergoing surgery between 2007–2012 and 2001–2006 (200 vs. 250 cc; P o 0.001), though with similar transfusion rates (16% vs. 14%; P ¼ 0.15). Positive surgical margins were likewise similar between the periods evaluated (2% vs. 3%; P ¼ 0.082) and median hospitalization length was lower in the latter period (4 vs. 3 d; P o 0.001). Univariable associations of the candidate predictors of interest with any early surgical complication and the multivariable model developed for this outcome are summarized in Table 3. There was evidence that the associations of the continuous versions of eGFR and Charlson score with a complication were not linear; as such, these features were categorized for analysis. In a multivariable setting, complication after PN was more likely in men (OR ¼ 1.40, P ¼ 0.036), when performed on a solitary kidney (OR ¼ 1.71; P ¼ 0.021) or in the setting of increasing comorbidity, as measured by the Charlson score (OR ¼ 1.97 for score Z3 compared with score 0; P o 0.001). Renal dysfunction (eGFR o 30) was also independently associated with postoperative complication (OR ¼ 2.89, P ¼ 0.002), as was increasing tumor size (OR ¼ 1.12 for each 1-cm increase in tumor size; P o 0.001). Surgical approach, specifically LPN and RPN, was associated with a lower odds of complication compared with OPN (OR ¼ 0.47, P ¼ 0.017 and OR ¼ 0.42, P ¼ 0.016).
4. Discussion In this comprehensive, contemporary update of 1,763 patients undergoing PN for sporadic renal masses, we have identified important patient-level factors associated with 30-day complications including surgery on a solitary kidney, baseline renal insufficiency, and increasing Charlson score. Importantly, 30-day complication rates remained stable between periods assessed (2001–2006 and 2007– 2012), with approximately 14% of patients experiencing at least one complication, including 7% of patients who experienced a Clavien grade 3, 4, or 5 event. Another important finding is the increased use of minimally invasive surgery at our institution, notably RPN, which mirrors national trends [7]. Reflecting likely selection bias, patients undergoing LPN or RPN tended to have smaller tumors, 2 kidneys, and fewer comorbidities. However, even when adjusting for surgical approach in a multivariable assessment, the aforementioned patient-level covariates all remained independently associated with 30day complications, though LPN and RPN were associated with a lower odds of complication. These data contribute additional context to discussions of how to best manage T1 renal masses, emphasizing patientlevel factors that may predict surgical complications after nephron-preserving surgery. Although PN offers excellent long-term oncologic and renal function outcomes [3], increasing attention has been placed on nonsurgical management in well-selected patients. This includes active surveillance in those with significant comorbidities and
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Table 2 Comparison of blood loss, complications, and positive surgical margins by year of surgery. Sample sizes for features with missing data are indicated in italics in parentheses Feature
All N ¼ 1,773
2001–2006 N ¼ 766 Median (IQR)
2007–2012 N ¼ 1,007
P Value
Blood loss, cc (N ¼ 1,707)
200 (100–450)
200 (100–400)
o0.001
Received blood transfusion Early complications (N ¼ 1,759) Death within 30 d Hemorrhage DVT PE MI Wound infection or dehiscence Abscess Urine leak Sepsis Acute renal failure Loss of kidney Additional surgical procedure Pneumothorax Any of the above Clavien grade(s) of complication (N ¼ 1,759) 1 2 3 4 5 3, 4, or 5
258 (15)
250 (100–500) N (%) 122 (16)
136 (14)
0.15
2 (o1) 65 (4) 6 (o1) 4 (o1) 14 (1) 33 (2) 17 (1) 77 (4) 11 (1) 65 (4) 1 (o1) 2 (o1) 16 (1) 241 (14)
2 (o1) 18 (2) 3 (o1) 0 7 (1) 20 (3) 10 (1) 31 (4) 6 (1) 34 (4) 1 (o1) 2 (o1) 4 (1) 104 (14)
0 47 (5) 3 (o1) 4 (o1) 7 (1) 13 (1) 7 (1) 46 (5) 5 (1) 31 (3) 0 0 12 (1) 137 (14)
0.19 0.009 1.0 0.14 0.62 0.044 0.20 0.57 0.55 0.14 0.43 0.19 0.14 0.94
102 (6) 59 (3) 86 (5) 41 (2) 2 (o1) 119 (7)
42 (6) 34 (4) 29 (4) 22 (3) 2 (o1) 47 (6) Median (IQR) 4 (3–5) N (%) 16 (2)
60 25 57 19 0 72
0.64 0.025 0.064 0.18 0.19 0.38
Length of hospital stay, d
4 (3–5)
Positive surgical margins (N ¼ 1,766)
51 (3)
(6) (3) (6) (2) (7)
3 (2–5) 35 (3)
o0.001 0.082
DVT ¼ deep vein thrombosis; IQR ¼ interquartile range; MI ¼ myocardial infraction; PE ¼ pulmonary embolism.
limited life expectancy, or percutaneous ablation for highrisk surgical candidates seeking definitive local management [10]. Indeed, we recently published our institutional experience on 180 patients undergoing radiofrequency and 187 patients undergoing cryoablation for T1 renal masses, and noted recurrence-free survival to be similar to PN [4]. Differences in overall survival in this study were felt to be related to nononcologic causes, owing to selection bias of unhealthier patients for percutaneous ablation. Complications after percutaneous ablation have been noted to be acceptably low in 2 recent series, reported between 15.2% and 17% [11,12]. However, direct comparison with PN is difficult owing to differences in patient characteristics [13] and must be interpreted carefully in the setting of any observational study design given concerns about selection bias of patients for nonsurgical interventions. Percutaneous ablation may also offer renal preservation akin to PN [14], and it has been demonstrated to be generally safe even in solitary kidneys [15,16]. Our results add to those presented by Larcher et al. [17], which included Charlson score, renal insufficiency, and tumor size as predictors of complications in a cohort of
2,476 patients undergoing PN in the Surveillance, Epidemiology, and End Results (SEER) registry. However, our findings differ in several key aspects. Overall 30-day complication rates were 27% in this SEER analysis, compared with 14% in our institutional analysis; however, this lower observed complication rate likely reflects our experience and high volume with PN. Indeed, the relationship between high-volume centers and favorable outcomes after PN have been described previously, including lower complication and mortality rates [18]. Furthermore, our data identified male sex and solitary kidney as independent risk factors for postoperative complication. The association of male sex on adverse surgical outcomes has unclear etiology, though an interaction between male sex and complications in urologic surgery has been described previously [19,20], in addition to an association between male sex and adherent perinephric fat during PN [21]. Short- and long-term complications after PN in solitary kidneys have been described in prior institutional series, with complication rates nearing 26% [22]. In this particular series, the association of solitary kidney and complications is likely multifactorial, including higher tumor complexity that is
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Table 3 Univariable and multivariable associations with an early surgical complication Feature
Univariable
Multivariable
OR (95% CI) Year of surgery 2001–2006 2007–2012 Age at surgery, y Sex Female Male Solitary kidney eGFR, mL/min/1.73 m2 Z60 Z45 to o60 Z30 to o45 o30 ECOG performance status 0 Z1 Charlson score 0 1 2 Z3 Obesity Type of PN Open Laparoscopic Robotic-assisted laparoscopic Tumor size, cm Histologic subtype Benign RCC
P value
OR (95% CI)
P value
1.0 (reference) 1.01 (0.77–1.33) 1.04 (0.93–1.16)a
0.94 0.49
1.0 (reference) 1.46 (1.09–1.96) 2.52 (1.67–3.79)
0.012 o0.001
1.0 (reference) 1.40 (1.02–1.91) 1.71 (1.09–2.70)
0.036 0.021
1.0 1.03 2.08 4.25
(reference) (0.70–1.52) (1.35–3.21) (2.28–7.92)
0.87 o0.001 o0.001
1.0 0.83 1.51 2.89
(reference) (0.55–1.25) (0.95–2.42) (1.48–5.62)
0.36 0.085 0.002
1.0 (reference) 2.08 (1.36–3.17)
o0.001
1.0 1.22 1.37 2.53 1.06
(reference) (0.81–1.82) (0.94–2.01) (1.78–3.60) (0.80–1.40)
0.34 0.10 o0.001 0.68
1.0 1.06 1.29 1.97
(reference) (0.69–1.63) (0.86–1.92) (1.33–2.91)
0.79 0.22 o0.001
1.0 0.46 0.35 1.15
(reference) (0.27–0.80) (0.18–0.68) (1.09–1.22)b
0.006 0.002 o0.001
1.0 0.47 0.42 1.12
(reference) (0.25–0.87) (0.21–0.85) (1.06–1.20)b
0.017 0.016 o0.001
1.0 (reference) 1.66 (1.13–2.45)
0.010
ECOG ¼ Eastern Cooperative Oncology Group; RCC ¼ renal cell carcinoma. OR and 95% CI represent a 10-year increase in age. b OR and 95% CI represent a 1-cm increase in tumor size. a
unfortunately not captured in our institutional registry with nephrometry scores. Lastly, renal insufficiency has been associated with perioperative complications even in the general surgery literature and has been postulated to be related to a number of different etiological mechanisms including impaired would healing and association with other significant comorbidities such as diabetes and cardiovascular disease [23]. Although the overall complication rate was noted to be approximately 14% here, for most patients evaluated, PN did appear to be safe and associated with excellent outcomes. Indeed, this included decreasing hospitalization length and lower blood loss observed between the 2 periods (2001–2006 and 2007–2012), likely influenced by the advent and expansion of RPN. Regardless, these favorable outcomes notwithstanding, the data here present a unique opportunity to better understand key covariates associated with short-term complications and may aid in patient counseling, surgical planning, and selection of management strategy for individual patients in the era of comparative effectiveness [24]. Future prospective studies
comparing the periprocedural morbidity after ablation and surgery would aid further in these discussions, though would continue to be a joint decision between the surgeon and patient. Even though these data are comprehensive, we must highlight important limitations of this study. First, its retrospective, single-institution design introduces ascertainment and referral bias, including of patients with high tumor complexity and increasing comorbidity. Indeed, our institutional experience with renal surgery also limits the generalizability of these results to smaller centers or community practices. Furthermore, there is potential for unmeasured and residual confounding, evening in the multivariable models we presented. That is, for example, although we do report on tumor size and adjust for this, we did not have data on tumor complexity (nephrometry scores) in our registry, which may be associated with postoperative complications. Indeed, increasing tumor complexity, especially in those patients with a “mandatory” indication for PN—such as solitary kidney—may increase surgical complexity and thus perioperative morbidity.
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5. Conclusion Several patient-level factors are associated with 30-day complications after PN, regardless of surgical approach. These data may inform counseling before PN, including potential identification and selection of high-risk surgical candidates for percutaneous ablative approaches.
[12]
[13]
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Original article
Patient factors associated with 30-day complications after partial nephrectomy: A contemporary update Harras B. Zaid, M.D.a, William P. Parker, M.D.a, Christine M. Lohse, M.S.b, John C. Cheville, M.D.c, Stephen A. Boorjian, M.D.a, Bradley C. Leibovich, M.D.a, R. Houston Thompson, M.D.a,* b
a Department of Urology, Mayo Clinic and Mayo Medical School, Rochester, MN Department of Health Sciences Research, Mayo Clinic and Mayo Medical School, Rochester, MN c Department of Pathology, Mayo Clinic and Mayo Medical School, Rochester, MN
Received 5 July 2016; received in revised form 20 October 2016; accepted 4 November 2016
Abstract Introduction: Patient-level factors associated with perioperative complications after partial nephrectomy (PN) have not been well described in a contemporary series. Methods: Single-institution retrospective study evaluating patients undergoing open, laparoscopic, and robotic PN between 2001 and 2012. Univariable and multivariable logistic regression models were evaluated to assess factors associated with complications within 30 days of surgery. Results: We identified 1,763 patients who underwent 1,773 PNs between 2001 and 2012. From 2001 to 2006, 766 PNs were performed (85% open, 15% laparoscopic, and o1% robotic); in contrast, from 2007 to 2012, 1,007 PNs were performed (75% open, 8% laparoscopic, and 17% robotic); P o 0.001. Overall, 241 (14%) PNs resulted in an early surgical complication. Patients undergoing a minimally invasive approach had smaller tumors (P o 0.001), were less likely to have a solitary kidney (P o 0.001), and had a lower Charlson score (P ¼ 0.004). On multivariable analysis, factors independently associated with an increased risk of any complication included male sex (odds ratio [OR] ¼ 1.40), solitary kidney (OR ¼ 1.71), estimated glomerular filtration rate (OR ¼ 2.89 for estimated glomerular filtration rate o30), Charlson score (OR ¼ 1.97 for Charlson score Z3), and tumor size (OR ¼ 1.12 for each 1-cm increase in tumor size); meanwhile, laparoscopic and robotic approaches were associated with a lower risk for complication (OR ¼ 0.017 and 0.016, respectively), all P o 0.05. Conclusion: Several patient-level factors are associated with 30-day complications after PN, regardless of surgical approach. These data may inform counseling before PN, including potential identification and selection of high-risk surgical candidates for percutaneous ablative approaches. r 2016 Elsevier Inc. All rights reserved.
Keywords: Complication; Laparoscopic; Partial nephrectomy; Percutaneous ablation; Robotic; Outcomes
1. Introduction Radical nephrectomy has historically been the treatment of choice for localized renal cell carcinoma. However, nephron-sparing surgery including open partial nephrectomy (OPN), laparoscopic partial nephrectomy (LPN), and robotic partial nephrectomy (RPN) are now favored for the management of T1 masses. Indeed, American Urological Association (AUA) and European Association of Urology Corresponding author. Tel.: þ1-507-266-9968; fax: þ1-507-284-4951. E-mail address: [email protected] (R.H. Thompson). *
http://dx.doi.org/10.1016/j.urolonc.2016.11.001 1078-1439/r 2016 Elsevier Inc. All rights reserved.
(EAU) guidelines encourage nephron preservation when technically feasible [1,2]. These recommendations are based partly on mounting evidence that partial nephrectomy (PN), compared with radical nephrectomy, may decrease the risk of chronic kidney disease [3]. Although PN still remains the treatment of choice in healthier patients [2], percutaneous ablation and surveillance may be selected in certain patients with competing comorbidities [4]. However, PN is often technically more challenging than radical nephrectomy and remains underused in the community despite perceived benefits [5,6]. Over the past 2 decades, practice patterns have also changed, with
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progressive shift from OPN to minimally invasive approaches [7]. The advent of robotics, furthermore, has augmented laparoscopy to make minimally invasive PN more technically accessible to practicing urologists [8]. As treatment patterns continue to change, comprehensive comparative data comparing OPN with minimally invasive PN are lacking [9]. Furthermore, although minimally invasive approaches have been demonstrated to be safe [7], few studies have documented patient-level risk factors influencing outcomes in those undergoing PN, adjusting for surgical approach. Indeed, a better understanding of these risk factors could potentially inform preoperative counseling and help identify patients who may be candidates for surveillance or percutaneous ablative approaches. Herein, we describe our institutional experience with PN from 2001 to 2012, a contemporary cohort, to comprehensively evaluate patient-level factors associated with 30-day perioperative morbidity. 2. Patients and methods
surgical procedure, and pneumothorax. Pathologic features included tumor size and histologic subtype (renal cell carcinoma or benign). 2.3. Statistical methods Continuous features were summarized with medians and interquartile ranges; categorical features were summarized with frequency counts and percentages. We compared features between an early cohort (2001–2006) and a later cohort (2007–2012) to assess temporal trends in practice patterns using Wilcoxon rank-sum, chi-square, and Fisher exact tests, where appropriate. Associations with any early surgical complication were evaluated using logistic regression models and summarized with odds ratios (ORs) and 95% CIs. A multivariable model was developed using stepwise selection with the P value for a feature to enter or leave the model set to 0.05. Statistical analyses were performed using version 9.3 of the SAS software package (SAS Institute, Cary, NC). All tests were two-sided and P o 0.05 were considered statistically significant.
2.1. Patient selection
3. Results
After institutional review board approval, we queried the Mayo Clinic Nephrectomy Registry to identify 1,763 patients who underwent 1,773 PNs for solid renal masses between 2001 and 2012. Patients with bilateral synchronous disease, von Hippel-Lindau syndrome, or tuberous sclerosis syndrome, were excluded.
A comparison of clinical, surgical, and pathologic features by year of surgery (2001–2006 vs. 2007–2012) is shown in Table 1. As can be seen, patients undergoing PN between 2007 and 2012 tended to be younger with higher eGFRs, have lower Charlson and ECOG scores, and present less frequently with tumors in a solitary kidney (all P o 0.05). Between 2001 and 2006, 766 PNs were performed (85% open, 15% laparoscopic, and o1% robotic); in contrast, between 2007 and 2012, 1,007 PNs were performed (75% open, 8% laparoscopic, and 17% robotic); P o 0.001. When compared with OPN, patients undergoing a minimally invasive approach had smaller tumors (2.2 vs. 3.2 cm; P o 0.001), were less likely to have a solitary kidney (3% vs. 9%; P o 0.001), and had lower Charlson scores (0 vs. 1; P ¼ 0.004). A full list of early complications is included in Table 2. No patient died intraoperatively. There were 241 (14%) PNs that resulted in an early surgical complication, with a similar rate regardless of period (P ¼ 0.94). Overall, 119 (7%) PNs experienced a Clavien grade 3, 4, or 5 complication, which was similar between 2001–2006 and 2007– 2012 (6% vs. 7%, P ¼ 0.38). With the exception of hemorrhage (2% vs. 5%; P ¼ 0.009) and wound infection or dehiscence (3% vs. 1%, P ¼ 0.044), other complications were similar between 2001–2006 and 2007–2012. To better evaluate these bleeding complications, hemorrhage events were stratified by surgical approach and were similar between OPN (n ¼ 54, 4%) and minimally invasive PN (n ¼ 11, 3%), P ¼ 0.48. Furthermore, wound dehiscence occurred only in
2.2. Clinical, surgical, and pathologic features Clinical features included year of surgery, age at surgery, sex, estimated glomerular filtration rate (eGFR) at diagnosis calculated using the Chronic Kidney Disease Epidemiology Collaboration formula, Eastern Cooperative Oncology Group (ECOG) performance status at surgery, Charlson score at surgery, and obesity (defined as body mass index Z30). Surgical features included approach to PN (open— OPN, laparoscopic—LPN, or robotic—RPN), surgical margin status, estimated blood loss, transfusion rates, length of hospital stay, and complications within 30 days of surgery including death, hemorrhage (defined as bleeding resulting in an intervention such as reoperation or angioembolization, or a hematoma confirmed on imaging), deep vein thrombosis, pulmonary embolism, myocardial infarction, wound infection or dehiscence (defined as infection requiring antibiotics or drainage, or a separation of the layers of the surgical wound requiring intervention), abscess (defined as abscess requiring antibiotics or drainage), urine leak, sepsis (defined as bacteremia that resulted in hypotension or admission to the intensive care unit), acute renal failure, loss of kidney, need for an additional
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Table 1 Comparison of baseline features by year of surgery. Sample sizes for features with missing data are indicated in italics in parentheses Feature
Age at surgery, y eGFR, mL/min/1.73 m2; (N ¼ 1,741) Charlson score (N ¼ 1,768) Tumor size, cm; (N ¼ 1,750) Sex Female Male Solitary kidney ECOG performance status (N ¼ 1,769) 0 Z1 Type of PN Open Laparoscopic Robotic-assisted laparoscopic Histologic subtype Benign RCC Obese (N ¼ 1,734)
All N ¼ 1,773
2001–2006 N ¼ 766 Median (IQR)
2007–2012 N ¼ 1,007
P value
60 79 0 3.0
o0.001 o0.001 o0.001 0.080
661 (37) 1,112 (63) 136 (8)
62 (53–71) 64 (51–75) 1 (0–2) 3.0 (2.0–4.2) N (%) 275 (36) 491 (64) 76 (10)
386 (38) 621 (62) 60 (6)
0.29
1,632 (92) 137 (8)
692 (90) 73 (10)
940 (94) 64 (6)
0.014
1,407 (79) 196 (11) 170 (10)
649 (85) 115 (15) 2 (o1)
758 (75) 81 (8) 168 (17)
o0.001
355 (20) 1,418 (80) 752 (43)
147 (19) 619 (81) 291 (40)
208 (21) 799 (79) 461 (46)
0.45
61 72 1 3.0
(52–68) (58–86) (0–2) (2.0–4.3)
(51–67) (66–93) (0–2) (2.1–4.4)
0.002
0.009
ECOG ¼ Eastern Cooperative Oncology Group; IQR ¼ interquartile range; RCC ¼ renal cell carcinoma.
patients undergoing OPN (n ¼ 33, 2%), with no such events in patients undergoing minimally invasive PN (P o 0.001). Median blood loss was significantly lower in patients undergoing surgery between 2007–2012 and 2001–2006 (200 vs. 250 cc; P o 0.001), though with similar transfusion rates (16% vs. 14%; P ¼ 0.15). Positive surgical margins were likewise similar between the periods evaluated (2% vs. 3%; P ¼ 0.082) and median hospitalization length was lower in the latter period (4 vs. 3 d; P o 0.001). Univariable associations of the candidate predictors of interest with any early surgical complication and the multivariable model developed for this outcome are summarized in Table 3. There was evidence that the associations of the continuous versions of eGFR and Charlson score with a complication were not linear; as such, these features were categorized for analysis. In a multivariable setting, complication after PN was more likely in men (OR ¼ 1.40, P ¼ 0.036), when performed on a solitary kidney (OR ¼ 1.71; P ¼ 0.021) or in the setting of increasing comorbidity, as measured by the Charlson score (OR ¼ 1.97 for score Z3 compared with score 0; P o 0.001). Renal dysfunction (eGFR o 30) was also independently associated with postoperative complication (OR ¼ 2.89, P ¼ 0.002), as was increasing tumor size (OR ¼ 1.12 for each 1-cm increase in tumor size; P o 0.001). Surgical approach, specifically LPN and RPN, was associated with a lower odds of complication compared with OPN (OR ¼ 0.47, P ¼ 0.017 and OR ¼ 0.42, P ¼ 0.016).
4. Discussion In this comprehensive, contemporary update of 1,763 patients undergoing PN for sporadic renal masses, we have identified important patient-level factors associated with 30-day complications including surgery on a solitary kidney, baseline renal insufficiency, and increasing Charlson score. Importantly, 30-day complication rates remained stable between periods assessed (2001–2006 and 2007– 2012), with approximately 14% of patients experiencing at least one complication, including 7% of patients who experienced a Clavien grade 3, 4, or 5 event. Another important finding is the increased use of minimally invasive surgery at our institution, notably RPN, which mirrors national trends [7]. Reflecting likely selection bias, patients undergoing LPN or RPN tended to have smaller tumors, 2 kidneys, and fewer comorbidities. However, even when adjusting for surgical approach in a multivariable assessment, the aforementioned patient-level covariates all remained independently associated with 30day complications, though LPN and RPN were associated with a lower odds of complication. These data contribute additional context to discussions of how to best manage T1 renal masses, emphasizing patientlevel factors that may predict surgical complications after nephron-preserving surgery. Although PN offers excellent long-term oncologic and renal function outcomes [3], increasing attention has been placed on nonsurgical management in well-selected patients. This includes active surveillance in those with significant comorbidities and
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Table 2 Comparison of blood loss, complications, and positive surgical margins by year of surgery. Sample sizes for features with missing data are indicated in italics in parentheses Feature
All N ¼ 1,773
2001–2006 N ¼ 766 Median (IQR)
2007–2012 N ¼ 1,007
P Value
Blood loss, cc (N ¼ 1,707)
200 (100–450)
200 (100–400)
o0.001
Received blood transfusion Early complications (N ¼ 1,759) Death within 30 d Hemorrhage DVT PE MI Wound infection or dehiscence Abscess Urine leak Sepsis Acute renal failure Loss of kidney Additional surgical procedure Pneumothorax Any of the above Clavien grade(s) of complication (N ¼ 1,759) 1 2 3 4 5 3, 4, or 5
258 (15)
250 (100–500) N (%) 122 (16)
136 (14)
0.15
2 (o1) 65 (4) 6 (o1) 4 (o1) 14 (1) 33 (2) 17 (1) 77 (4) 11 (1) 65 (4) 1 (o1) 2 (o1) 16 (1) 241 (14)
2 (o1) 18 (2) 3 (o1) 0 7 (1) 20 (3) 10 (1) 31 (4) 6 (1) 34 (4) 1 (o1) 2 (o1) 4 (1) 104 (14)
0 47 (5) 3 (o1) 4 (o1) 7 (1) 13 (1) 7 (1) 46 (5) 5 (1) 31 (3) 0 0 12 (1) 137 (14)
0.19 0.009 1.0 0.14 0.62 0.044 0.20 0.57 0.55 0.14 0.43 0.19 0.14 0.94
102 (6) 59 (3) 86 (5) 41 (2) 2 (o1) 119 (7)
42 (6) 34 (4) 29 (4) 22 (3) 2 (o1) 47 (6) Median (IQR) 4 (3–5) N (%) 16 (2)
60 25 57 19 0 72
0.64 0.025 0.064 0.18 0.19 0.38
Length of hospital stay, d
4 (3–5)
Positive surgical margins (N ¼ 1,766)
51 (3)
(6) (3) (6) (2) (7)
3 (2–5) 35 (3)
o0.001 0.082
DVT ¼ deep vein thrombosis; IQR ¼ interquartile range; MI ¼ myocardial infraction; PE ¼ pulmonary embolism.
limited life expectancy, or percutaneous ablation for highrisk surgical candidates seeking definitive local management [10]. Indeed, we recently published our institutional experience on 180 patients undergoing radiofrequency and 187 patients undergoing cryoablation for T1 renal masses, and noted recurrence-free survival to be similar to PN [4]. Differences in overall survival in this study were felt to be related to nononcologic causes, owing to selection bias of unhealthier patients for percutaneous ablation. Complications after percutaneous ablation have been noted to be acceptably low in 2 recent series, reported between 15.2% and 17% [11,12]. However, direct comparison with PN is difficult owing to differences in patient characteristics [13] and must be interpreted carefully in the setting of any observational study design given concerns about selection bias of patients for nonsurgical interventions. Percutaneous ablation may also offer renal preservation akin to PN [14], and it has been demonstrated to be generally safe even in solitary kidneys [15,16]. Our results add to those presented by Larcher et al. [17], which included Charlson score, renal insufficiency, and tumor size as predictors of complications in a cohort of
2,476 patients undergoing PN in the Surveillance, Epidemiology, and End Results (SEER) registry. However, our findings differ in several key aspects. Overall 30-day complication rates were 27% in this SEER analysis, compared with 14% in our institutional analysis; however, this lower observed complication rate likely reflects our experience and high volume with PN. Indeed, the relationship between high-volume centers and favorable outcomes after PN have been described previously, including lower complication and mortality rates [18]. Furthermore, our data identified male sex and solitary kidney as independent risk factors for postoperative complication. The association of male sex on adverse surgical outcomes has unclear etiology, though an interaction between male sex and complications in urologic surgery has been described previously [19,20], in addition to an association between male sex and adherent perinephric fat during PN [21]. Short- and long-term complications after PN in solitary kidneys have been described in prior institutional series, with complication rates nearing 26% [22]. In this particular series, the association of solitary kidney and complications is likely multifactorial, including higher tumor complexity that is
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Table 3 Univariable and multivariable associations with an early surgical complication Feature
Univariable
Multivariable
OR (95% CI) Year of surgery 2001–2006 2007–2012 Age at surgery, y Sex Female Male Solitary kidney eGFR, mL/min/1.73 m2 Z60 Z45 to o60 Z30 to o45 o30 ECOG performance status 0 Z1 Charlson score 0 1 2 Z3 Obesity Type of PN Open Laparoscopic Robotic-assisted laparoscopic Tumor size, cm Histologic subtype Benign RCC
P value
OR (95% CI)
P value
1.0 (reference) 1.01 (0.77–1.33) 1.04 (0.93–1.16)a
0.94 0.49
1.0 (reference) 1.46 (1.09–1.96) 2.52 (1.67–3.79)
0.012 o0.001
1.0 (reference) 1.40 (1.02–1.91) 1.71 (1.09–2.70)
0.036 0.021
1.0 1.03 2.08 4.25
(reference) (0.70–1.52) (1.35–3.21) (2.28–7.92)
0.87 o0.001 o0.001
1.0 0.83 1.51 2.89
(reference) (0.55–1.25) (0.95–2.42) (1.48–5.62)
0.36 0.085 0.002
1.0 (reference) 2.08 (1.36–3.17)
o0.001
1.0 1.22 1.37 2.53 1.06
(reference) (0.81–1.82) (0.94–2.01) (1.78–3.60) (0.80–1.40)
0.34 0.10 o0.001 0.68
1.0 1.06 1.29 1.97
(reference) (0.69–1.63) (0.86–1.92) (1.33–2.91)
0.79 0.22 o0.001
1.0 0.46 0.35 1.15
(reference) (0.27–0.80) (0.18–0.68) (1.09–1.22)b
0.006 0.002 o0.001
1.0 0.47 0.42 1.12
(reference) (0.25–0.87) (0.21–0.85) (1.06–1.20)b
0.017 0.016 o0.001
1.0 (reference) 1.66 (1.13–2.45)
0.010
ECOG ¼ Eastern Cooperative Oncology Group; RCC ¼ renal cell carcinoma. OR and 95% CI represent a 10-year increase in age. b OR and 95% CI represent a 1-cm increase in tumor size. a
unfortunately not captured in our institutional registry with nephrometry scores. Lastly, renal insufficiency has been associated with perioperative complications even in the general surgery literature and has been postulated to be related to a number of different etiological mechanisms including impaired would healing and association with other significant comorbidities such as diabetes and cardiovascular disease [23]. Although the overall complication rate was noted to be approximately 14% here, for most patients evaluated, PN did appear to be safe and associated with excellent outcomes. Indeed, this included decreasing hospitalization length and lower blood loss observed between the 2 periods (2001–2006 and 2007–2012), likely influenced by the advent and expansion of RPN. Regardless, these favorable outcomes notwithstanding, the data here present a unique opportunity to better understand key covariates associated with short-term complications and may aid in patient counseling, surgical planning, and selection of management strategy for individual patients in the era of comparative effectiveness [24]. Future prospective studies
comparing the periprocedural morbidity after ablation and surgery would aid further in these discussions, though would continue to be a joint decision between the surgeon and patient. Even though these data are comprehensive, we must highlight important limitations of this study. First, its retrospective, single-institution design introduces ascertainment and referral bias, including of patients with high tumor complexity and increasing comorbidity. Indeed, our institutional experience with renal surgery also limits the generalizability of these results to smaller centers or community practices. Furthermore, there is potential for unmeasured and residual confounding, evening in the multivariable models we presented. That is, for example, although we do report on tumor size and adjust for this, we did not have data on tumor complexity (nephrometry scores) in our registry, which may be associated with postoperative complications. Indeed, increasing tumor complexity, especially in those patients with a “mandatory” indication for PN—such as solitary kidney—may increase surgical complexity and thus perioperative morbidity.
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5. Conclusion Several patient-level factors are associated with 30-day complications after PN, regardless of surgical approach. These data may inform counseling before PN, including potential identification and selection of high-risk surgical candidates for percutaneous ablative approaches.
[12]
[13]
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