Vol.

45 (5): 932-940, September - October, 2019

ORIGINAL ARTICLE
doi: 10.1590/S1677-5538.IBJU.2018.0776

Preoperative proteinuria is associated with increased rates

of acute kidney injury after partial nephrectomy
_______________________________________________
Önder Kara 1, 2, Matthew J. Maurice 1, Pascal Mouracade 1, Ercan Malkoc 1, Julien Dagenais 1, Mustafa
Çapraz 3, Jaya S. Chavali 1, Merve Yazici Kara 4, Jihad H. Kaouk 1
1
Department of Urology, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, OH, USA;
2
Kocaeli University, Medical School, Kocaeli, Turkey; 3 Amasya University, Medical School, Amasya,
Turkey; 4 Kocaeli Derince Training and Research Hospital, Kocaeli, Turkey

ABSTRACT ARTICLE INFO

Purpose: We investigated the association between preoperative proteinuria and early Önder Kara
postoperative renal function after robotic partial nephrectomy (RPN). https://orcid.org/0000-0003-1197-2932
Patients and Methods: We retrospectively reviewed 1121 consecutive RPN cases at a
single academic center from 2006 to 2016. Patients without pre-existing CKD (eGFR≥60 Keywords:
mL/min/1.73m2) who had a urinalysis within 1-month prior to RPN were included. The Kidney Neoplasms; Proteinuria;
cohort was categorized by the presence or absence of preoperative proteinuria (trace or Acute Kidney Injury
greater (≥1+) urine dipstick), and groups were compared in terms of clinical and func-
Int Braz J Urol. 2019; 45: 932-40
tional outcomes. The incidence of acute kidney injury (AKI) was assessed using RIFLE
criteria. Univariate and multivariable models were used to identify factors associated
with postoperative AKI. _____________________
Results: Of 947 patients, 97 (10.5%) had preoperative proteinuria. Characteristics as- Submitted for publication:
sociated with preoperative proteinuria included non-white race (p<0.01), preoperative November 22, 2018
diabetes (p<0.01) and hypertension (HTN) (p<0.01), higher ASA (p<0.01), higher BMI _____________________
(p<0.01), and higher Charlson score (p<0.01). The incidence of AKI was higher in pa- Accepted after revision:
tients with preoperative proteinuria (10.3% vs. 4.6%, p=0.01). The median eGFR pres- January 13, 2019
ervation measured within one month after surgery was lower (83.6% vs. 91%, p=0.04) _____________________
Published as Ahead of Print:
in those with proteinuria; however, there were no significant differences by 3 months
March 20, 2019
after surgery or last follow-up visit. Independent predictors of AKI were high BMI
(p<0.01), longer ischemia time (p<0.01), and preoperative proteinuria (p=0.04).
Conclusion: Preoperative proteinuria by urine dipstick is an independent predictor of
postoperative AKI after RPN. This test may be used to identify patients, especially those
without overt CKD, who are at increased risk for developing AKI after RPN.

INTRODUCTION been an upward trend in the utilization of robo-

tic partial nephrectomy (RPN) for the treatment
Partial nephrectomy (PN) is the gold stan- of renal masses, and relatedly robotic adoption
dard treatment for T1a, and when technically has increased the overall utilization of nephron-
feasible T1b renal masses, due to improved re- -sparing surgery (2, 3). PN reduces the amount
nal functional preservation (1). Given the be- of renal parenchymal volume loss, more so when
nefits offered by the robotic platform, there has performed robotically; however; it does not eli-

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minate nephron loss entirely (4-6). Furthermore, (trace or greater (≥1+) urine dipstick), and absen-
the remaining kidney may experience ischemic ce (negative urine dipstick).
damage as a result of the temporary vascular
clamping required during PN (5). Acute kidney Definition of AKI
injury (AKI) is associated with increased hospi- The diagnosis of AKI was based on RIFLE
tal length of stay and in hospital mortality (7), criteria (16). Grade 1 (risk) is characterized by a
and following AKI patients have an increased 1.5-2.0-fold increase in serum creatinine or urine
risk of residual structural and functional disease output (UO)<0.5mL/kg/h for 6 hours; grade 2 (in-
(8). Therefore, preoperative prediction of AKI, jury) is characterized by a 2.0-3.0-fold increase in
especially for patients with presumed normal serum creatinine or UO 0.5mL/kg/h for 12 hours;
renal function (Estimated Glomerular Filtration grade 3 (failure) is characterized by any increase
Rate (eGFR)>60) is difficult, and important in >3.0-fold in serum creatinine, temporary need for
patients’ counseling. dialysis, UO <0.3mL/kg/h for 12 hours, or anuria
The glomerular filtration rate (GFR) has for 12 hours. There were no cases of renal loss or
been used for a long time as the primary indica- end-stage renal failure in this cohort of patients.
tor in diagnosing and staging CKD (9). However,
Kidney Disease Improving Global Outcomes (KDI- Study variables
GO) recently included etiology, eGFR, and protei- Demographic and tumor characteristics
nuria as vital components for CKD identification, included patient age; race (white and non-white);
as each of them has a prognostic value on survi- gender; body mass index (BMI); Charlson Comor-
val and renal function stability in the population bidity Index (CCI); American Society of Anesthe-
(10-12). The association between CKD severity siology (ASA) score; history of preoperative dia-
and AKI risk after PN was quantified based on one betes mellitus (DM), hypertension (HTN), and/or
component of KDIGO classification (as measured smoking; preoperative estimated glomerular fil-
by levels of estimated GFR) in previously publi- tration rate (eGFR); solitary kidney status; tumor
shed series (13-15). Our primary objective was to size; R.E.N.A.L. score; and tumor pathology (be-
assess proteinuria as a marker of early renal dys- nign or malignant). Intraoperative variables inclu-
function in patients undergoing RPN. ded operative time, ischemia time, estimated blood
loss (EBL), and intraoperative transfusion. Posto-
PATIENTS AND METHODS perative variables included 30-day postoperative
complications, length of hospital stay, and 30-day
Using our institutional review board-ap- readmissions. Complications were graded using
proved database, we abstracted data on 1121 RPN the Clavien-Dindo classification system (17) and
cases performed at our center from 2006 to 2016. were characterized as minor (Clavien 1-2) and ma-
Patients without pre-existing CKD (eGFR≥60 jor (Clavien 3-5). Tumor complexity was assessed
mL/min/1.73m2) who had a urinalysis within based on the R.E.N.A.L nephrometry classification
1-month prior to RPN were included in the study system (18). Functional outcomes were assessed
(n=947). The cohort was categorized by the pres- using eGFR, which was calculated using the mo-
ence or absence of preoperative proteinuria, and dification of diet in renal disease (MDRD) formula
groups were compared in terms of clinical and (19). eGFR preservation was defined as follow-up
functional outcomes. The incidence of AKI was postoperative eGFR divided by baseline eGFR x
assessed using RIFLE criteria. Univariate and 100. CKD upstaging was defined as any increase in
multivariable models were used to identify fac- CKD stage (20) from the time of preoperative asses-
tors associated with postoperative AKI. sment to the time of latest postoperative follow-up.

Definition of proteinuria Surgical technique

Urine dipstick analysis was used to detect We used our standard RPN technique as
proteinuria. Proteinuria was defined as presence described previously (21). The transperitoneal

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approach was used in all cases. Intraoperative vs. 4.6%, p=0.01). The median eGFR preserva-
ultrasound was used routinely for intraoperati- tion measured within one month after surgery
ve tumor identification and surgical planning. was lower (83.6 (73.3-89.8) % vs. 91 (79-101) %,
Intracorporeal renal parenchymal cooling was p=0.04) in those with proteinuria; however, there
used selectively when ischemia times were ex- were no significant differences by 3 months af-
pected to be greater than 25 minutes. ter surgery (88 (77.3-98.4) % vs. 89 (78.2-97.5) %,
p=0.9) or last follow-up visit (85.1 (72.9-96.2) %
Study outcomes vs. 86.9 (76.1–98.2) %, p=0.2). Likewise, the prev-
The primary outcome was postoperative AKI. alence of CKD upstaging at the latest follow-up
AKI was assessed using RIFLE criteria. Univariate and (19.5 vs. 18.7 months, p=0.56) did not differ be-
multivariable models were used to identify factors tween groups (43.3% vs. 42.1%, p=0.82) (Table-2).
associated with postoperative AKI. Secondary ou- In terms of secondary outcomes, there
tcomes included operative time, EBL, ischemia time, were no significant differences in intraoperative
perioperative transfusion, length of hospital stay, 30- variables, including operative time, EBL, ischemia
day readmission, overall and major complications. time, and intraoperative blood transfusion betwe-
en the two groups. However, proteinuria was as-
Statistical analysis sociated with higher rates of overall (26.8% vs.
16.8, p=0.01) and major (9.3% vs. 4.6%, p=0.04)
Continuous variables, presented as mean ± postoperative complications and 30-day readmis-
standard deviation (SD) if normally distributed or sions (Table-3).
as median (interquartile range (IQR)) if non-nor- On further analysis of postoperative com-
mally distributed, were compared using the t-test plications, the specific complications, which con-
or Mann-Whitney U test, respectively. Categorical tributed to the disparity in complication rates
variables were compared using the chi-squared test. between groups, included postoperative cardiac
Multivariable analysis was conducted using logis- complications (7.2% vs. 2.6, p=0.02), and haemor-
tic regression to identify independent predictors of rhagic complications necessitating selective ar-
postoperative AKI. Significance was set at p<0.05. terial angioembolisation (4.1% vs. 0.9%, p=0.02)
Analyses were performed using SPSS v24 software (Table-4).
(IBM SPSS Statistics, Armonk, NY: IBM Corp). On multivariable logistic regression, after
adjusting for BMI, CCI, preoperative proteinuria,
RESULTS tumor size, baseline eGFR, and ischemia time, sig-
nificant predictors of postoperative AKI included
In the final cohort, 947 patients were in- higher BMI (OR 1.07, 95% CI 1.03-1.17, p<0.01),
cluded. Preoperative proteinuria was observed ischemia time >20 min (OR 4.86, 95% CI 2.14-
in 97 (10.5%) patients on urine dipstick. Of the- 11.01) p<0.01), and preoperative proteinuria (OR
se, 18 (18.5%) had trace (<30 mg/dL), 78 (80.4%) 2.4, 95% CI 1.02-5.65, p=0.04) (Table-5).
had 30 to 299 mg/dL, and 1 (1.1%) had >300 mg/
dL urinary protein preoperatively. Characteristics DISCUSSION
associated with preoperative proteinuria included
non-white race (p<0.01), pre-existing DM (p<0.01), Despite the nephron-sparing benefits of
pre-existing HTN (p<0.01), higher BMI (p<0.01), PN, 4.9% of patients undergoing PN experience
higher ASA (p<0.01), and higher Charlson score postoperative AKI (15). In turn, AKI is associated
(p<0.01). Tumor characteristics, including mass with increased morbidity and mortality (22). Whi-
size (p=0.08), R.E.N.A.L score (p=0.13), and ma- le preexisting CKD is one of the most common
lignant disease (p=0.06), were not associated with risk factor for postoperative AKI after PN, even
preoperative proteinuria (Table-1). patients with normal preoperative renal function
Postoperative AKI was more prevalent are at risk for postoperative AKI (23). However, at
in patients with preoperative proteinuria (10.3% present, these at-risk patients without CKD are not

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Table 1 - Patient demographic and tumor characteristics. T

Variables Proteinuria P value

Yes No
N=97 (10.5%) N=850 (89.5%)

Age years, (±SD) 57.1 (12.7) 57.7 (12) 0.79

Gender 0.11

Male, n (%) 65 (67) 499 (58.7)

Female, n (%) 32 (33) 351 (41.3)

Race <0.01

White, n (%) 75 (77.3) 756 (89)

Non-White, n (%) 22 (22.7) 144 (11)

S
BMI, med (IQR) 31.2 (26.2-37) 29.3 (25.8-33.5) 0.04

ASA, med (IQR) 3 (3-3) 3 (2-3) <0.01

CCI, med (IQR) 1 (0-2) 0 (0-1) <0.01

Diabetes Mellitus, n (%) 29 (29.9) 154 (18.1) <0.01

Hypertension, n (%) 64 (66) 451 (53.1) 0.01

Smoker, n (%) 13 (13.4) 123 (14.5) 0.77

Pre-Op eGFR, med (IQR) 87.2 (71.3-102.2) 88.5 (76–100.5) 0.58

Solitary kidney, n (%) 3 (3.1) 13 (1.5) 0.22

Tumor size on CT cm, med (IQR) 3.4 (2.2-4.4) 3 (2.1-4) 0.08

R.E.N.A.L score, med (IQR) 8 (6–9) 7 (6–9) 0.13

Malignant disease, n (%) 86 (88.7) 682 (80.2) 0.06

BMI = Body mass index; CCI = Charlson comorbidity index; CKD = Chronic kidney disease; CT = Computed tomography; EBL = Estimated blood loss; eGFR = Estimated
glomerular filtration rate; IQR = Interquartile range; OPN = Open partial nephrectomy; RPN = Robotic partial nephrectomy; SD = Standard deviation

readily identifiable. Thus, there is a need for better have reported postoperative AKI rates after PN
tools to identify such patients who are more likely ranging from 0.8% to 10% (13, 15, 25) varying by
to experience AKI after PN. institution, technique, approach, data collection,
Proteinuria has been identified as an es- and AKI criteria. In our study, we used the RIFLE
sential component of renal dysfunction based classification scheme for AKI, which is generally
on the most recent KDIGO guidelines (12) and accepted for use in the PN population (24).
appears to be a significant and independent We found that proteinuria was an inde-
predictor of overall survival and recurrence free pendent risk factor for AKI in non-CKD patients
survival in patients undergoing renal cancer undergoing PN. Patients with proteinuria had
surgery (24). Therefore, we hypothesized that 2.4-fold higher odds of AKI than patients without
preoperative proteinuria may be associated with proteinuria. These results are consistent with prior
postoperative AKI. studies that have shown an association between
In this retrospective study, the prevalen- proteinuria and AKI after non-renal (26-28), and
ce of postoperative AKI was 5.1%. Some studies renal surgeries (29). Surprisingly, in our study, pre-

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Table 2 - Follow-up functional data.

Variables Proteinuria P value

Yes No
N=97 (10.5%) N=850 (89.5%)
Early postoperative functional outcomes (Primary Outcomes)
Acute kidney injury (RIFLE), n (%) 10 (10.3) 39 (4.6) 0.01
Risk (R) 9 (9.3) 35 (4.1)
Injury (I) 1(1) 4 (0.5)
Within 1 mo. eGFR, mL/min/1.73 m2, median 73 (63-90) 80 (69-98) 0.02
(IQR)
Within 1 mo. % eGFR preservation, median 83.6 (73.3-89.8) 91 (79-101) 0.04
(IQR)
Late postoperative functional outcomes
3-mo. eGFR, mL/min/1.73 m2, median (IQR) 76 (61-94.9) 77 (65.3-91.8) 0.98
3-mo. % eGFR preservation, median (IQR) 88 (77.3-98.4) 89 (78.2-97.5) 0.9
Follow up times, months, median (IQR) 19.5 (6.2-29.4) 18.7 (5.7-38.4) 0.56
Latest eGFR, mL/min/1.73 m2, median (IQR) 72 (61.1–89.1) 76 (64.3–90.4) 0.12
Latest follow up % eGFR preservation, median 85.1 (72.9–96.2) 86.9 (76.1–98.2) 0.2
(IQR)
CKD upstaging at last follow-up, n (%) 42 (43.3) 358 (42.1) 0.82
IQR = Interquartile range; SD = Standard deviation

Table 3 - Secondary outcomes.

Variables Proteinuria P value

Yes No
N=97 (10.5%) N=850 (89.5%)
Intraoperative outcomes
Operation time, min, mean (±SD) 182 (48.8) 180 (53) 0.34
EBL, mL., med (IQR) 150 (100-300) 150 (100-250) 0.92
Ischemia time, min, mean (±SD) 20.8 (10) 20.3 (10.1) 0.68
Intraoperative transfusion, n (%) 2 (2.1) 7 (0.8) 0.23
Perioperative outcomes
Length of stay, days, med, (IQR) 3 (2-4) 3 (2-4) 0.23
30-day readmission, n (%) 8 (8.2) 31 (3.6) 0.03
Postoperative transfusion, n (%) 2 (2.2) 48 (5.9) 0.22
Overall C. (Clavien-Dindo 1-5), n (%) 26 (26.8) 143 (16.8) 0.01
Major C. (Clavien-Dindo 3-5), n (%) 9 (9.3) 39 (4.6) 0.04

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Table 4 - Summary of complications based on preoperative proteinuria.

Proteinuria P value
Complication type, % (n) Yes No
N=97 (10.5%) N=850 (89.5%)
Overall complications 26 (26.8) 143 (16.8) 0.01
Major (Clavien-Dindo 3-5) 9 (9.3) 39 (4.6) 0.04
Cardiac complications 7 (7.2) 22 (2.6) 0.02
Myocardial infarction 1 (1) 0 (0)
Arrhythmia 4 (4.1) 16 (1.9)
Other cardiac 2 (2.1) 6 (0.7)
Pulmonary complications 4 (4.1) 51 (6) 0.64
Pneumonia 1 (1) 9 (1.1)
DVT/PE 1 (1) 11 (1.3)
Other pulmonary 2 (2.1) 31 (3.6)
Genitourinary complications 3 (3.1) 13 (1.5) 0.22
UTI 2 (2.1) 4 (0.5)
Urine leak 1 (1) 9 (1.1)
Gastrointestinal complications 5 (5.2) 32 (3.8) 0.41
Clostridium difficil infection 1 (1) 1 (0.1)
Ileus/small bowel obstruction 3 (3.1) 29 (3.4)
Other gastrointestinal 1 (1) 2 (0.2)
Wound complications 2 (2.1) 18 (2.1) 1
Surgical site infection 0 (0) 13 (1.5)
Hernia 0 3 (0.4)
Other wound 2 (2.1) 2 (0.2)
Neurologic complications 0 2 (0.2) 1
Bleeding complications 9 (6.3) 11 (14.1)
Postop Transfusion 2 (2.1) 48 (5.6) 0.22
Need for angioembolisation 4 (4.1) 8 (0.9) 0.02

operative proteinuria was not a predictor of long- is quick, inexpensive, and widely available, making
-term renal functional preservation. This finding it a good screening test. Preoperative assessment
contrasts a study by Krane et al. (30) and Bhindi et of proteinuria may help guide preoperative patient
al. (29), and O’Donnell et al. (31) which did show counseling, postoperative care, and medical treat-
an association between proteinuria and long-term ment in non-CKD PN patients.
risk of CKD. It is possible that our follow up was In addition to proteinuria, longer ischemia
not long enough to detect a difference in long- time and higher BMI were also independent risk
-term functional outcomes. factors for AKI. Our study demonstrated a 4.8-fold
Our findings suggest that proteinuria de- higher risk of AKI in patients with ischemia times
tected on urine dipstick is a good predictor of pos- longer than 20 minutes. The association between
toperative AKI in non-CKD patients. Urine dipstick longer ischemia time and increased risk of post-PN

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Table 5 - Logistic regression analysis predicting AKI after PN.

Variables Univariate Multivariate

OR 95 % CI P OR 95 % CI P

Age (per year) 0.99 0.97-1.01 0.3

Race

(White vs. Non-White) 0.66 0.3-1.45 0.4

Gender (Male vs. Female 1.01 0.56-1.82 0.95

BMI (per kg/m2) 1.07 1.04-1.11 <0.01 1.07 1.03-1.11 <0.01

CCI (per unit) 1.21 0.98-1.49 0.01 1.19 0.95-1.48 0.12

Hypertension (yes vs.no) 1.34 0.74-2.42 0.32

Diabetes (yes vs.no) 1.37 0.7-2.7 0.34

Proteinuria (yes vs. no) 2.3 1.15-4.95 0.01 2.4 1.02-5.65 0.04

Tumor size (per cm) 1.28 1.11-1.47 <0.01 1.05 0.87-1.27 0.55

Baseline eGFR (per mL/min/1.73m2) 1.01 0.99-1.02 0.11 1.01 0.99-1.02 0.07

Ischemia time ≤20 min. Ref Ref

Ischemia time >20 min 4.63 2.13-10.4 <0.01 4.86 2.14-11.01 <0.001

EBL (per cc) 1 1-1 0.38

IVF during surgery 1 1-1 0.57

CI = Confidential interval; EBL = Estimated Blood Loss; OR = Odds ratio

AKI is well established in the literature (32-34). In vergent populations (36).

terms of patient factors, BMI was the only indepen- Our study is not without limitations. The
dent predictor of post-PN AKI. Obesity has been retrospective design is a potential source of bias,
identified previously as a risk factor for AKI after and results from this single tertiary-care center co-
surgery, consistent with our results (35). The patho- hort may not be generalizable. While multivariable
physiology of obesity-associated AKI is poorly un- analysis was used to adjust for known risk factors
derstood but may be related to comorbidities, such for postoperative AKI, additional unmeasured fac-
as DM and HTN. tors, for which we could not adjust, may have in-
Our study suggests an increased risk of fluenced the ultimate risk of AKI. Another limitation
overall and major complications and 30-day read- is that urine dipstick was used rather than 24-hour
missions following PN in patients with proteinuria. urinalysis for the assessment of proteinuria. Althou-
This association did not persist on multivariable lo- gh a 24-hour urinalysis would be the ideal study for
gistic regression analysis, suggesting that comorbid proteinuria, it is a more expensive and cumbersome
conditions, which occur commonly together with test that would not be practical in all patients un-
proteinuria, may be responsible for this increased dergoing PN.
morbidity. Specifically, postoperative cardiovascu-
lar complications were more common in patients CONCLUSIONS
with proteinuria, consistent with prior studies that
have shown an association between proteinuria and Our results indicate that preoperative pro-
cardiovascular morbidity and mortality across di- teinuria by urine dipstick is an independent pre-

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dictor of postoperative AKI after RPN in non-CKD 7. Chertow GM, Soroko SH, Paganini EP, Cho KC, Himmelfarb
patients. This test may be used to identify patients J, Ikizler TA, et al. Mortality after acute renal failure: models
with occult renal dysfunction who are at increased for prognostic stratification and risk adjustment. Kidney Int.
risk for developing post-PN AKI. 2006;70:1120-6.
8. Chawla LS, Eggers PW, Star RA, Kimmel PL. Acute kidney
Compliance with Ethical Standards injury and chronic kidney disease as interconnected
syndromes. N Engl J Med. 2014;371:58-66.
Dr. Jihad H. Kaouk is a consultant for En- 9. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic
docare/HealthTronics, and Intuitive. No compe- kidney disease and the risks of death, cardiovascular events,
ting financial interests exist for the other authors. and hospitalization. N Engl J Med. 2004;351:1296-305.
Erratum in: N Engl J Med. 2008;18:4.
ACKNOWLEDGEMENTS 10. Stevens PE, Levin A; Kidney Disease: Improving Global
Outcomes Chronic Kidney Disease Guideline Development
Dr. Önder Kara and Dr. Ercan Malkoç were Work Group Members. Evaluation and management of
supported by a grant for life expenses from TU- chronic kidney disease: synopsis of the kidney disease:
BITAK: Technology and Innovation Support Pro- improving global outcomes 2012 clinical practice guideline.
grams, Directorate of the Scientific and Research Ann Intern Med. 2013;158:825-30.
Council of Turkey. 11. Lane BR, Demirjian S, Derweesh IH, Riedinger CB, Fergany
AF, Campbell SC. Is all chronic kidney disease created equal?
CONFLICT OF INTEREST Curr Opin Urol. 2014;24:127-34.
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None declared. Terreni A, ET AL.F. KDIGO 2012 Clinical Practice Guideline
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