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DOI: 10.4081/aiua.2023.

12130

ORIGINAL PAPER

Oncological and functional outcomes of patients who


underwent open partial nephrectomy for kidney tumor
Efe Bosnali 1, Enes Abdullah Baynal 2, Naci Burak Cinar 2, Enes Malik Akdas 2, Engin Telli 2,
Büsra Yaprak Bayrak 3, Kerem Teke 2, Hasan Yilmaz 2, Ozdal Dillioglugil 2, Onder Kara 2
1 Universityof Health Sciences, Derince Training and Research Hospital, Department of Urology, Kocaeli, Turkey;
2 Kocaeli University, School of Medicine, Department of Urology, Kocaeli, Turkey;
3 Kocaeli University, School of Medicine, Department of Pathology, Kocaeli, Turkey.

Summary Objective: To report long-term functional and INTRODUCTION


oncological outcomes of OPN Renal cell cancer (RCC) incidence is rising in Western
Methods: We enrolled 182 patients who underwent consecutive countries and accounts for approximately 3% of adult
OPN with a diagnosis of kidney tumor in our clinic between cancers (1). During the last two decades, nephron-sparing
April 2002 and February 2020 and were selected from our surgery (NSS) has become the standard for managing
prospective OPN database. Preoperative demographic and clini- localized renal tumors, achieving excellent oncological
cal characteristics, intraoperative and pathological results, and outcomes and functional preservation (2). Long-term
patients' postoperative functional and oncological follow-up data oncological results of OPN in masses smaller than 4 cm
were retrospectively analyzed. Overall survival (OS) and dis-
have been well-defined, and it has been reported that
ease-free survival (DFS) were evaluated using Kaplan-Meier
similar results are obtained with radical nephrectomy (RN)
survival analysis. The time-dependent variation between preop-
erative and postoperative functional results was statistically ana- in local recurrence, disease free survival (DFS), and metas-
lyzed and presented in a graph. tasis-free survival (3, 4). The purpose of PN is to protect
Results and limitations: The mean age was 54.4 ± 10.8 yr, and the maximum kidney tissue without compromising onco-
the median age-adjusted Charlson comorbidity index (ACCI) logical principles, thereby reducing kidney failure and
was 1 (interquartile range [IQR] 0-1). The mean tumor size was related cardiac problems that may develop at various lev-
3.1 ± 1.2 cm, and the median RENAL score was 6 (IQR 5-8). The els and extending the OS times compared to RN (5). With
most common malign histopathological subtype was clear cell the increase in the diagnosis of incidental masses, interest
carcinoma with 76.6%, and five cases (3.4%) had positive surgi- in NSS has increased. In the National Comprehensive
cal margins (PSMs). The most common surgical techniques were Cancer Network (NCCN) and EAU guidelines, PN is rec-
the retroperitoneal approach (98.9%) and cold ischemia (88.5%). ommended to treat early-stage renal tumors under any
Estimated glomerular filtration rate (eGFR) preservation was technically feasible condition (6). We presented our
92% (80.8-99.3, IQR), which translates to 32% chronic kidney experience of single-center OPN, including long-term
disease (CKD) upstaging. Acute kidney injury (AKI) was detect- functional and oncological outcomes, in describing the
ed in 27 (14.8%) patients according to RIFLE criteria. The intra- complications and rates that developed during and after
operative complication rate was 5.5%, and the postoperative surgery.
overall complication rate (Clavien-Dindo 1-5) was 30.2%. Major
complications (Clavien-Dindo 3-5) were observed in 13 (7.1%)
patients. The median oncological follow-up was 42 mo (21.3- MATERIALS AND METHODS
84.6, IQR), and the 5- and 10-yr OS were 90.1% and 78.6%, 5
and 10-yr DFS were 99.4% and 92.1%, respectively. No local
Patient selection
recurrence was observed in 5 (3.4%) patients with PSMs; only
A retrospective analysis of the prospective OPN database
one had distant metastasis in the 8th postoperative month. The
retrospective design, the small number of patients who under- approved by our institutional review board was per-
went PN based on mandatory indication, and one type of surgi- formed in May 2020. All consecutive patients undergoing
cal approach may limit the generalizability of our findings. surgery between April 2002 and February 2020 were
Conclusions: This study confirms excellent long-term oncologic selected. Five surgeons experienced in OPN performed
and functional outcomes after OPN in a cohort of patients select- the surgeries. Due to limited access to the previous hos-
ed from a single institution. In light of the information provided pital patient record system, patients who underwent open
by the literature and our study, our recommendation is to push PN between 1996 and 2001 were excluded. Overall, 182
the limits of PN under every technically feasible condition in the patients were included in this study.
treatment of kidney tumors to protect the kidney reserve and
achieve near-perfect oncological results. Variables
Preoperative demographic and clinical data of the
KEY WORDS: Kidney tumor; Open Partial Nephrectomy;
Functional outcomes; Oncological outcomes. patients included age, gender, race, body mass index
(BMI), age-adjusted Charlson comorbidity index (ACCI),
Submitted 25 November 2023; Accepted 30 November 2023 American society of anesthesiologists (ASA) score, history of

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

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E. Bosnali, E. Abdullah Baynal, N. Burak Cinar, et al.

diabetes and hypertension, previous abdominal surgery tional imaging in postoperative follow-up. Local recur-
and smoking status, presence of a solitary kidney, and rence was defined as detecting a new enhancing lesion in
preoperative eGFR. the surgical bed or the same renal space. Distant metasta-
Tumor complexity was graded as low (RENAL score 4-6, sis was defined as disease recurrence in the contralateral
PADUA score 6-7), moderate (RENAL score 6-9, PADUA kidney or other body organs.
score 8-9), or high (RENAL score 10-12, PADUA score
10-14). Clinical UICC-TNM stage and nephrometry Surgical technique
scores could not be determined in 51 patients whose pre- We used the previously described standard OPN surgical
operative cross-sectional imaging could not be accessed. method in all patients. The most common surgical tech-
Intraoperative variables included surgical approach and nique in the study was the retroperitoneal flank approach
technique (ureteral stenting), operative time, estimated (98.9%) and cold ischemia (88.5%). Depending on the
blood loss (EBL), ischemia type, cold ischemia time (CIT), tumor's location, a subcostal incision was made parallel
warm ischemia time (WIT), use of a hemostatic agent, to the 11th or 12th rib. The kidney was mobilized entire-
transfusion rate, and intraoperative complications. ly with the surrounding Gerota fascia, and the renal pedi-
Postoperative variables included length of hospital stay cle was exposed.
(LoS), 30-day readmission rate, and types of postopera- In order to prevent ischemic kidney damage and reduce
tive complications and their incidence. Postoperative intracellular edema, 16 grams of 20% mannitol solution
complications were graded using the Clavien-Dindo clas- was given intravenously to all patients who underwent
sification, with grade 3a or higher considered major com- cold ischemia a few minutes before arterial clamping.
plications. Patients with acute kidney ınjury (AKI) were Then, by placing a bulldog clamp on the renal artery,
determined based on the RIFLE criteria for creatinine and renal hypothermia was induced by intracorporeal ice
eGFR values in the first week postoperatively. Urine leak- melting for 15 minutes. Three different (cold, hot, zero)
age was defined as a creatinine value ≥ 2 mg /dl in the ischemia types were preferred. While mannitol and ice
drain fluid in addition to postoperative follow-up for at slush application were not applied in the warm ischemia
least 4 days or a significant collection around the kidney group, a clamp was not placed on the renal artery in the
in postoperative radiological examinations. zero ischemia group. Tumor tissue was excised in a
Tumor histology was performed according to the 2004 wedge shape with a scalpel and cold scissors, leaving
World Health Organization criteria, and grade classifica- approximately 3-5 mm of normal renal parenchyma
tion followed the Fuhrman/International Society of around it, preserving the overlying fat tissue. 3/0
Urological Pathology (ISUP) scheme. The 2017 yr Union absorbable polyglactin sutures were used to close the
for International Cancer Control (UICC)-TNM classifica- defect that may develop in the collecting system after
tion system was used for pathological staging. PSM was excision and to provide hemostasis due to bleeding. After
defined as an extension of tumor to the inked surface of achieving hemostasis, the bulldog clamp was removed,
the resected specimen on final pathology. and the duration of cold or warm ischemia was recorded.
The preserved fatty tissue was wrapped and sutured (with
Follow up absorbable suture material) in oxidized regenerated cellu-
Renal function assessment was based on serum eGFR lose (Surgicel) or polyglactin (Vicryl) mesh and placed
measurements postoperative days 1 and 3 at regular into the bed of the defect.
intervals of 1, 3, 6, and 12 months. The time difference The fatty tissue was wrapped in order to provide the
between the preoperative and final eGFR dates of the appropriate shape for the defect after excision and to help
patients constituted the functional follow-up period. hemostasis with the effect of foreign materials around it.
eGFR was estimated using the Chronic Kidney Disease Blunt-tipped non-traumatic 1/0 absorbable polyglactin
Epidemiology Collaboration (CKD-EPI) equation and CKD sutures were passed through the renal parenchyma along
staging were assigned according to the eGFR value based the edges of the defect and tied separately, and the
on the NKF-KDOQI guideline. eGFR preservation was wrapped fat tissue was fixed to the resection bed, and
calculated as the proportion of postoperative eGFR was renorrhaphy was completed.
measured at the last follow-up to preoperative eGFR, and
rates of CKD upstaging were evaluated (upstaging from Statistical analysis
class I-II to III-V, class III to IV-V, or class IV to V). The normal distribution of variables was evaluated with
Oncological outcomes were evaluated through routine the Kolmogorov-Smirnov test.
postoperative follow-up cross-sectional imaging studies, Mean ± standard deviation (SD) was used for parametric
e.g., CT of the chest, abdominal CT and/or MRI. Imaging variables, and median and interquartile range (IQR) values
was carried out at 6, 12 months, then yearly and when were used for nonparametric variables. The median eGFR
clinically indicated. Postoperative cross-sectional imaging values in the preoperative and postoperative follow-ups
and medical records of the patients were examined, and were compared in pairs using the nonparametric
the presence of local recurrence or distant metastasis and Friedman test. The time-dependent change of postopera-
the causes of death were included in oncological follow- tive eGFR was shown with a Box and whisker plot graph.
up data. Overall survival (OS) was defined as the time OS and DFS analyses for 5 and 10 years were performed
between the date of surgery and the date of death (all using the Kaplan-Meier method. All statistical analyses
causes). Disease-free survival (DFS) was defined as the were performed using SPSS v24 software (IBM SPSS
period between the date of surgery and the date of local Statistics, Armonk, NY: IBM Corporation, USA). P < 0.05
recurrence or distant metastasis diagnosed by cross-sec- was considered statistically significant.

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

2
Long-term oncological and functional outcomes of open partial nephrectomy

Table 1. Table 2.
Patient’s Demographics and Preoperative Data. Preoperative tumor characteristics and R.E.N.A.L. Score Details.
Variables Total OPN (n = 182) Tumor size, cm, mean (±SD) 3.1 (± 1.2)
Age years, mean (± SD) 54.4 (± 10.8) Side, right, n (%) 110 (60.4)
Male, n (%) 79 (43.4) Clinical UICC-TNM stage, n (%)
White race, n (%) 182 (100) T1a 108 (82.4)
BMI, mean (± SD) 28.3 (± 5.3) T1b 18 (13.7)
CCI, med (IQR) 1 (0-1) T2 0
ASA, med (IQR) 2 (2-2) T3a 5 (3.8)
Diabetes, n (%) 51 (28) Cystic Lesion, n (%) 46 (33.1)
Hypertension, n (%) Hilar Location, n (%) 4 (3)
No 92 (50.5) Total Number of Arteries, n (%)
Yes 90 (49.5) 1 155 (88.1)
Controlled 81 (44.5) >1 21 (11.9)
Non controlled 9 (5) N/A, n 6
Smoker, n (%) CSA, cm2, med (IQR) 11 (6.7–19.7)
No 115 (63.2) R.E.N.A.L score, med (IQR) 6 (5–8)
Yes 55 (30.2) R.E.N.A.L Complexity, n (%)
Former 12 (6.6) Simple (4-6) 81 (61.8)
Prior Abdominal Surgery, n (%) 48 (26.4) Intermediate (7-9) 48 (36.6)
Pre-op Hb g/dl, mean (± SD) 13.7 (± 1.5) Complex (10-12) 2 (1.5)
Solitary Kidney, n (%) 6 (3.3) ®adius (max diameter in cm), n (%)
Pre-op eGFR, med (IQR) 96 (82.4-105.9) ≤4 146 (81.6)
> 4 but < 7 31 (17.3)
Pre-op CKD stages, n (%)
≥7 2 (1.1)
I. (eGFR ≥ 90 ml/min/1.73 m2) 113 (62.1)
II. (eGFR 60-89 ml/min/1.73 m2) 53(29.1) (E)xophytic/Exophytic Properties, n (%)
IIIa. (eGFR 45-59 ml/min/1.73 m2) 7 (3.8) ≥ 50% 67 (51.2)
IIIb. (eGFR 30-44 ml/min/1.73 m2) 5 (2.7) < 50% 57 (43.5)
IV. (eGFR 15-29 ml/min/1.73 m2) 2 (1.1) Entirely endophytic 7 (5.3)
(N)earness of The Tumor to the Collecting System or Renal Sinus (mm), n (%)
ASA, American Society of Anesthesiologists; BMI, Body mass index; CCI, Charlson comorbidity index;
CKD, Chronic kidney disease; eGFR, Estimated glomerular filtration rate; Hb, Hemoglobin; IQR, Interquartile range; ≥7 59 (45)
OPN, Open partial nephrectomy; SD, Standard deviation. > 4 but < 7 41 (31.3)
≤4 31 (23.7)
(L)ocation Relative to the Polar Lines (points), n (%)
1 71 (54.2)
2 35 (26.7)
RESULTS
3 25 (19.1)
CSA, Contact surface area; IQR, Interquartile range; SD, Standard deviation.
Patients’ characteristics

In total, 182 OPNs were performed during this initial


time frame for our OPN experience. cases had zero ischemia; the mean WIT for the remaining
The mean age at surgery was 54.4 ± 10.8 yr, and 56.6% of patients was 26.1 ± 7.7 minutes. The median operative
patients were women. Six (3.3%) patients underwent PN time was 240 min (IQR 180-240), and the median EBL
for a solitary kidney tumor, and 4 (2.1%) patients pre- was 400 ml (IQR 300-600). The intraoperative complica-
sented with bilateral renal neoplasms requiring PN. tion rate was 5.5%, and renal vein injury was the most
Median preoperative eGFR was 96 ml/min/1.73 m2 CKD- common (1.7%). The intraoperative transfusion rate was
EPI (7.6% of patients had preoperative CKD stage ≥ 3). 28.6%.
The demographic and preoperative data are presented in The intraoperative data are summarized in Table 4.
Table 1.
The mean tumor size on preoperative imaging (CT or Postoperative and pathological outcomes
MRI) was 3.1±1.2 cm, and 82.4% of neoplasms were clas- The median postoperative LoS was 5 days (IQR 4-7). The
sified as clinical stage T1a. Median RENAL and PADUA postoperative overall complication rate was 30.2%, and
scores were 6 (IQR 5-8) and 7 (IQR 7-9), respectively. pulmonary complications were the most common
According to the RENAL and PADUA nephrometry scor- (9.3%). Major complications (Clavien-Dindo grade ≥ 3)
ing systems, 38.1% and 49.6% of tumors were classified were observed in 13 (7.1%) patients (Table 5). Urinary
as moderately to highly complex, respectively. Seven leakage occurred in 3.2% of cases and pseudo-aneurysm
(5.3%) patients had completely endophytic tumors. The in 1.1% of the patients. According to the RIFLE criteria,
preoperative characteristics of the tumors are presented AKI was detected in 27 (14.8%) patients. No patients
in Table 2 and Table 3. required postoperative hemodialysis during follow-up.
Postoperative complications are detailed in Table 6.
Intraoperative outcomes Final histopathologic analysis revealed clear cell RCC in
The retroperitoneal approach (98.9%) and cold ischemia 81% of cases. Most tumors (78%) were classified as pT1a
(88.5%) were the most common surgical techniques. Six and 16.2% were of high Fuhrman/ISUP grade (3 or 4).

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

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E. Bosnali, E. Abdullah Baynal, N. Burak Cinar, et al.

Table 3. Table 5.
Preoperative Tumor Characteristics and PADUA Score Details. Postoperative Data of The Patients.

PADUA score, med (IQR) 7 (7–9) Variables Total OPN (n = 182)


PADUA Complexity, n (%) Length of Stay (LoS), days, med (IQR) 5 (4-7)
Simple (6-7) 66 (50.4) Postoperative Transfusion, n (%) 14 (7.7)
Intermediate (8-9) 42 (32.1)
ES Units, med (IQR) 2 (1-2.2)
Complex (10-14) 23 (17.5)
Tumor Size (max diameter in cm), n (%) Overall Postop Complications, n (%) 55 (30.2)
≤4 146 (81.6) Major (Clavien-Dindo 3-5) Postop Complications 13 (7.1)
> 4 but < 7 31 (17.3) Minor (Clavien-Dindo 1-2) Postop Complications 41 (23.1)
≥7 2 (1.1) Readmission for Urologic Reasons, n (%) 11 (6)
Exophytic Rate, n (%) < 30 days 7 (3.8)
≥ 50% 67 (51.2) ≥ 30 days 4 (2.2)
< 50% 57 (43.5)
ES, Erythrocyte suspension; IQR, Interquartile range; OPN, Open partial nephrectomy.
Entirely endophytic 7 (5.3)
Tumor Relationship with Renal Sinus, n (%)
Absent relationship 114 (87)
With renal sinus location 17 (13) Table 6.
Tumor Relationship with Urinary Collecting System, n (%)
Postoperative Complication Type of The Patients.
Absent relationship 76 (58)
Dislocated/Infiltrated 55 (42) Postoperative Complication Type Total OPN (n = 182)
Renal Rim Location, n (%) Cardiac Complications, n (%) 3 (1.6)
Not involved 101 (77.1) 1 Hypertension 2 (1.1)
Involved 30 (22.9) 2 Cyanosis 1 (0.5)
Location Relative to the Sinus Lines (points), n (%) Pulmonary Complications, n (%) 17 (9.3)
1 79 (60.3) 1 Atelectasis (Need for Antibiotics) 14 (7.6)
2 52 (39.7) 2 Pleural Effusion 3 (1.6)
IQR, Interquartile range; PADUA, (P)reoperative (A)spects and (D)imensions used for an (A)natomical. Genitourinary Complications, n (%) 16 (8.7)
1 Urine Leakage 14 (7.6)
2 Perirenal/Psoas Abscess 2 (1.1)
Table 4.
Bleeding Complications, n (%) 16 (8.7)
Intraoperative Data of The Patients.
1 Postoperative Transfusion 14 (7.6)
Variables Total OPN (n = 182) 2 Need for Angioembolization 2 (1.1)
Surgical Approach, n (%) Other Infections (Use of Antibiotics), n (%) 4 (2.2)
Retroperitoneal 180 (98.9) Ileus/ Small Bowel Obstruction, n (%) 2 (1.1)
Transperitoneal 2 (1.1)
Hernia, n (%) 4 (2.2)
Operation Time, min, med (IQR) 240 (180-240)
Acute Kidney Injury (RIFLE Criteria), n (%) 27 (14.8)
Double J Stent, n (%)
Routinely 95 (52.2) R Risk (Increased Cre x 1,5 or eGFR decrease > %25) 23 (12.6)
As required (intra-operative) 14 (7.7) I Injury (Increased Cre x 2 or eGFR decrease > %50) 4 (2.2)
No 73 (40.1) F Failure (Increased Cre x 3 or eGFR decrease ≥ %75) 0
EBL, ml., med (IQR) 400 (300-600) L Loss (Complete loss of renal function ≥ 4 weeks) 0
Management of Renal Pedicle, n (%) E End stage renal disease 0
Off clamp 6 (3.3)
Global clamp 176 (96.7)
Technique of Ischemia, n (%)
Warm 15 (8.2) Five (3.4%) patients had PSMs. Among the benign
Cold 161 (88.5) pathologies, oncocytoma was reported most frequently
Zero 6 (3.3) (70.6%). The pathological data of the patients are pre-
Ischemia Time, min, mean (±SD) 26.1 (± 7.7) sented in Table 7.
Warm 19.4 (± 3.5)
Cold 32.1 (± 4.9)
Use of Haemostatic Agents, n (%) 17 (9.3) Oncological and functional outcomes
Tissel 3 (1.6) The median oncological follow-up of the patients was 42
Floseal 12 (6.6) (IQR 21.3-84.6) mo. Local recurrence was observed in
Arista 2 (1.1) three (1.6%) patients at the postoperative 63rd, 73rd and
Intraoperative Complications, n (%) 10 (5.5) 89th mo. respectively. Distant metastasis developed in 4
1 cm size injury to the proximal ureter 1 (0.5)
Serosal injury to the colon 1 (0.5)
(2.2%) patients at 8th, 63rd, 64th, and 96th mo. after sur-
Injury to the renal vein 3 (1.6) gery secondary to RCC. Seventeen patients died (9.3%),
Pleural injury 1 (0.5) including one from renal cancer (0.5%). No local recur-
Laceration of the spleen 1 (0.5) rence was observed in 5 (3.4%) patients with PSMs.
Vascular injury in the vena cava 2 (1.1) Only one (0.5%) patient with PSMs had distant metasta-
Injury of the aberrant artery supplying the lower pole 1 (0.5)
sis in the 8th postoperative mo. The 5-and 10-yr OS were
Intraoperative Transfusion, n (%) 52 (28.6)
ES Units, med (IQR) 1 (1-2) determined as 90.1% and 78.6%, 5 and 10-yr DFS rates
EBL, Estimated blood loss; ES, Erythrocyte suspension; IQR, Interquartile range; SD, Standard deviation;
with the Kaplan-Meier method, respectively, were 99.4%
OPN, Open partial nephrectomy. and 92.1% (Figure 1). Oncological data are summarized
in Table 8.

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

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Long-term oncological and functional outcomes of open partial nephrectomy

Table 7. Table 8.
Pathological Data of The Patients. Oncological Outcomes and Follow-up Data of The Patients.
Variables Total OPN (n = 182) Follow-up Times (oncological), mo., med (IQR) 42 (21.3-84.6)
Malignant Disease, n (%) 145 (81) Local Recurrence, n (%) 3 (1.6)
Benign Disease, n (%) 34 (19) Time to Local Recurrence, mo., med (IQR) 73 (63-89)
N/A, n 3 Distant Metastasis, n (%) 4 (2.2)
Pathological UICC-TNM stage, n (%) Time to Distant Metastasis, mo., med (IQR) 63.5 (21.7-88)
T1a 120 ( 83.3)
Death, n (%) 5 (3.5)
T1b 21 (14.5)
RCC-Related Death, n (%) 1 (0.5)
T2a 0
T3a 3 (2.1)
N/A, n 1
Histological Subtype, n (%) Table 9.
Clear Cell 111 (76.6) Functional Outcomes and Follow-up Data of The Patients.
Papillary 25 (17.2)
Chromophobe 7 (4.8) Follow-up Times (functional), mo., med (IQR) 32.8 (12.3-71)
Malignant mezenchymal 1 (0.7) Preop eGFR, med (IQR) 96 (82.4-105.9)
Tubulocystic carcinoma 1 (0.7) Postop 1st day eGFR, med (IQR) 88.1 (70.3-100.3)
Benign Disease, n (%) 34 (19) Postop 1st day % eGFR preservation, med (IQR) 94.2 (81.9-100)
Histological Subtype, n (%) Postop 3rd day eGFR, med (IQR) 91.4 (73.8-101.4)
Oncocytoma 24 (70.6) Postop 3rd day % eGFR preservation, med (IQR) 95 (87.4-100.9)
Angiomyolipoma 5 (14.7) Postop 1st mo. eGFR, med (IQR) 91.1 (77.3-102)
Other benign types 5 (14.7)
Postop 1st mo. % eGFR preservation, med (IQR) 95.2 (86.3-100.6)
Positive Surgical Margin, n (%) 5 (3.4)
Postop 3rd mo. eGFR, med (IQR) 87.2 (70.4-100.2)
Fuhrman/ ISUP Grade, n (%)
Low FG (1-2) 113 (83.7) Postop 3rd mo. % eGFR preservation, med (IQR) 92.6 (82-99.2)
High FG (3-4) 24 (16.2) Postop 6th mo. eGFR, med (IQR) 87 (70.4-97)
N/A, n 10 Postop 6th mo. % eGFR preservation, med (IQR) 92.2 (83.2-99.2)
FG, Fuhrman grade; ISUP, International Society of Urological Pathology; OPN, Open partial nephrectomy. Postop 1st yr. eGFR, med (IQR) 87.3 (70.9-99.8)
Postop 1st yr. % eGFR preservation, med (IQR) 92.4 (82.2-99.3)
Latest eGFR, med (IQR) 86.8 (70.4-99.1)
Latest Follow up % eGFR preservation (IQR) 92.9 (80.8-99.3)
The median eGFR preservation after OPN was 92.9% Latest CKD Upstaging, n (%) 58 (32.2)
(IQR 80.8-99.3%), which translates to a CKD upstaging
rate of 32.2%. The median postoperative eGFR was 86.8
ml/min/1.73 m2; data for all patients were available with
a median interval of 32.8 mo (IQR 12.3-71) after surgery lesions. On the other hand, RN was chosen for high-com-
(Table 9). Time-dependent change between eGFR values plexity preoperative cases. It is known that long ischemia
in preoperative and postoperative follow-up was statisti- times in PN harm kidney function. It was well reported
cally analyzed using the Friedman test and demonstrated that irrespective of the surgical method, hot and cold
using a Box and whisker plot graph (Figure 2). ischemia should not take longer than 20 and 30-35 min-
utes, respectively (10). Thus, cold ischemia was advised to
be performed in the literature for cases requiring longer
DISCUSSION clamping times. In order to benefit from the advantages of
With an increased diagnosis of incidental masses, the cold ischemia, researchers from Cleveland Clinic defined
interest in NSS has increased and as a result, PN has been icing techniques that can be utilized during laparoscopic
suggested to be performed according to the NCCN and PN (LPN) and robotic-assisted PN (RAPN) for complex
EAU guidelines, irrespective of the surgery method, for cases (11). Yossepowitch et al. (12) demonstrate that while
the treatment of early-stage kidney tumors. CIT correlated with eGFR decrease immediately after sur-
In order to obtain good oncological and functional results gery, this correlation was no longer present 1 year after the
in PN, all uro-oncologists are required to know the indi- procedure, highlighting the impact of cold ischemia on
cations, technical details, and complications of PN as well preserving long-term kidney function in a study that
as its management by using the advantages of minimally included 592 cases of cold PN series with a median CIT of
invasive techniques. Currently, at least 50% of new RCCs 35 minutes. In our study, cold and hot ischemia was per-
are diagnosed incidentally and smaller than 4 cm. This is formed in 88.5% and 8.2% of our patients, respectively,
further supported by previous studies focused on high whereas zero ischemia was performed in 3.3%. The mean
number OPN series, which show mean tumor sizes of cold and hot ischemia times were 32.1 and 19.4 minutes,
2.7-3.4 cm (7, 8). Despite this regression, concerning pre- respectively, within the previously suggested range; there-
vious years, the more extensive lesions, centrally located fore, we envision comparable and normal long-term kid-
and related to the collecting system, were chosen to per- ney function for both cohorts.
form OPN (9). In our study, the mean preoperative tumor A 2020 meta-analysis study, comparing OPN and LPN
size was 3,1 ± 1.2 cm) and RENAL and PADUA scores from 26 different studies with 8095 cases, did not show
showed that over half of the tumors are low-complexity any differences in intraoperative complication rate and

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

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E. Bosnali, E. Abdullah Baynal, N. Burak Cinar, et al.

Figure 1.
Kaplan-Meier curves
of the survival of
patients undergoing
open partial
nephrectomy.
(A) Overall survival.
(B) Disease-free
survival.

operation time between these two methods. However, it The rate of general complications in various PN series
was reported that LPN decreased the EBL, LoS, and blood varies between 4.1-38.6% in previous studies (4, 7, 15),
transfusion requirements (13). In another study compar- with urine leakage and bleeding as the most frequent
ing OPN, LPN, and RAPN performed for tumors less than postoperative complications (7, 8). We found a general
4 cm, it was found that OPN led to increased surgery time (major and minor) complication rate of 30.2 %, with pul-
(199 ± 56 min) and bleeding (168 ± 266 ml) compared monary complications (9.2%), bleeding (8.7%), and
to RAPN (174 ± 64 min, 84 ± 165 ml) (14). In our series, urine leakage (7.6%) being the most common. Chang et
the median operative time of 240 min and bleeding of al. (16) reported a major complication rate of 7.3% in
400 ml is greater than in previous reports. The routine 122 patients that resemble those in our study in terms of
ureteral stenting (52.2%), 15 minutes application of tumor characteristics and demographics. Thus, our post-
intracorporal ice slush treatment (88.5%), and additional operative major complication rate of 7.1% is in accor-
application of lipocorticoplasty could have contributed to dance with previous studies. An intraoperative complica-
the elongation of the operation time. tion rate of 3-5% was detected in the OPN series with a

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

6
Long-term oncological and functional outcomes of open partial nephrectomy

Figure 2.
Time-dependent change between eGFR values in preoperative and postoperative follow-up (Box and whisker plot graph).

high number of patients, with pleural injuries being the thus, temporary dialysis was deemed unnecessary. When
major case (17, 18). In our study, the rate of intraopera- compared with the literature, we think that the normal
tive complications was 5.5%, in accordance with the lit- preoperative renal function of most patients, the low num-
erature. ber of patients with high complexity lesions and solitary
AKI is observed in approximately 20% of all PN, nega- kidneys, utmost care on the maximum ischemia time, and
tively affecting long-term kidney function (19). Our study experience of open surgery in our clinic have contributed
defined AKI for RIFLE criteria for up to 3 days post-oper- to the low incidence of short-term kidney damage post-PN
ation (20). In a recent study, 25% of AKI was observed in and improved functional recovery in the long-term.
a cohort of 944 pT1 stage patients operated with three dif- A negative surgical margin is required to be left out fol-
ferent PN techniques by RIFLE criteria (21). We found an lowing tumor excision according to standard surgical
AKI of 14.8% in our study. This lower AKI rate could be principles. PSMs can be observed between 1.3-18% in
attributed to good preoperative kidney function and a OPN cohorts. When PN was carried out in large tumors
small number of solitary kidneys in our cohort. (> 4 cm) or complex tumors with mandatory indications,
Time-dependent decrease in renal function has been a higher rate of PSM was observed (23, 25). Even if, min-
extensively studied, primarily in bilateral kidneys. Kidney imally invasive strategies involving optical magnification
function was found to decrease post-PN immediately but and pedicule clamping with ischemia and tumor's cold
reached stable levels 3 weeks to 3 months after surgery scission, are advantageous with increased surgical experi-
upon partial recovery (22). Porpiglia et al. (23) followed ence, PSM was higher in large cohorts than in open sur-
the kidney function of patients with bilateral kidneys fol- geries (7). PSM rates were found to be 4.9, 8.1 and 8.7%
lowing LPN via scintigraphy. They found a significant in OPN, LPN, and RAPN, respectively, in a study includ-
recovery of kidney function 3 months post-operation. In ing more than 11500 cases with comparable numbers for
our study, when the postoperative eGFR was compared each PN (26). In minimally invasive techniques, the lack
with the preoperative eGFR in the time-dependent graph, of tactile sensations in determining the extension of the
a statistically significant loss of kidney function was found masses to the renal parenchyma at different axis angles
on the postoperative 1st day. The postoperative 3th day, and difficulty in determining the plan between the renal
we observed partial recovery of eGFR levels followed by parenchyma and the tumor border due to the use of ener-
stabilization of kidney function after 1 month, which was gy devices may cause higher rates of PSM compared to
in accordance with the results obtained by Porpiglia et al. open surgery. In our clinic, where all patients were sub-
CKD is defined as a heterogeneous distortion affecting the jected to OPN, PSM rate was 3.4%. In OPN, three-dimen-
structure and function of kidneys. NKF-KDOQ1 devel- sional masses extending into the renal parenchyma at dif-
oped this term in 2002, and the guides demonstrate that ferent axis angles can be clearly excised from the kidney
these distortions can elevate to life-threatening levels (24). and tumor border can be identified by means of tactile
In our cohort, primarily composed of cold ischemia senses and use of cold scissors, contributing to the lower
patients, we found 92.9% median preservation of final detection of PSM observed in our clinic.
eGFR levels during 32 months of functional follow-up; No local recurrence was observed in the close follow-up

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

7
E. Bosnali, E. Abdullah Baynal, N. Burak Cinar, et al.

of 5 (3.4%) patients with PSM. A distant metastasis was 2. Fergany AF, Hafez KS, Novick AC. Long-term results of nephron
detected in one (0.5%) at the postoperative 8th mo. PSM sparing surgery for localized renal cell carcinoma: 10-year follow-
was previously correlated with increased local recurrence up. J Urol. 2000; 163:442-5.
risk and distant metastasis progression (27). In another 3. Pahernik S, Roos F, Hampel C, et al. Nephron sparing surgery for
study with a median follow-up of 62 months, PSM was renal cell carcinoma with normal contralateral kidney: 25 years of
reported as an independent predictor of OS, RFS, and experience. J Urol. 2006; 175:2027-31.
DFS (28). Studies indicate that PSM does not influence
4. Patard J-J, Shvarts O, Lam JS, et al. Safety and efficacy of partial
survival; however, shorter follow-up and smaller cohort nephrectomy for all T1 tumors based on an international multicenter
sizes may not had the statistical power to determine experience. J Urolo. 2004; 171:2181-5.
PSM's effect (29, 30).
The objective of PN is to preserve the kidney tissue while 5. Thompson RH, Boorjian SA, Lohse CM, et al. Radical nephrectomy
adhering to oncological principles maximally, in order to for pT1a renal masses may be associated with decreased overall sur-
decrease the prevalence of different levels of kidney fail- vival compared with partial nephrectomy. J Urol. 2008; 179:468-73.
ure and related cardiac problems, and ultimately to 6. Kaouk JH, Autorino R. Laparoendoscopic single-site surgery
increase longevity compared to RN (5). Local recurrence (LESS) and nephrectomy: current evidence and future perspectives.
rates have been reported in the 1.4-3.3% range in large Eur Urol. 2012; 62:613-5
OPN cohorts with at least 5 yrs of follow-up (3, 31). Lane 7. Gill IS, Kavoussi LR, Lane BR, et al. Comparison of 1,800 laparo-
et al. (32) reported a 10-yr minimum OS of 72 and 78% scopic and open partial nephrectomies for single renal tumors. J Urol.
in 299 patients with OPN and LPN, respectively. 2007; 178:41-6.
Marszalek et al. (33) reported the oncological outcomes
of 100 age-, sex-, and tumor size-matched patients treat- 8. Patard J-J, Pantuck AJ, Crepel M, et al. Morbidity and clinical out-
come of nephron-sparing surgery in relation to tumour size and indi-
ed with OPN and LPN. In this study, the 5-yr OS were cation. Eur Urol. 2007; 52:148-54.
85% and 96%, and 5-yr DFS were 94% and 96.3%,
respectively. 9. Weight CJ, Fergany AF, Gunn PW, et al. The impact of minimal-
In our study, local recurrence was observed in 3 (1.6%) ly invasive techniques on open partial nephrectomy: a 10-year single
patients and a distant metastasis was observed in 4 institutional experience. J Urol. 2008; 180:84-8.
(2.1%) patients during a median of 42 (21.3-84.6, IQR) 10. Becker F, Van Poppel H, Hakenberg OW, et al. Assessing the
months of oncological follow-up. RCC-related death impact of ischaemia time during partial nephrectomy. Eur Urol.
occurred in one (0.5%) patient with distant metastasis. 5 2009; 56:625-35.
and 10-yr DFS were 99.4 and 99.2%. 5 and 10-yr OS 11. Ramirez D, Caputo PA, Krishnan J, et al. Robot-assisted partial
were 90.1 and 78.6%, respectively. Most of the tumors nephrectomy with intracorporeal renal hypothermia using ice slush:
belonging to the pT1a stage (83.3%) and with low step-by-step technique and matched comparison with warm
Fuhrman/ISUP grade (83.7%) combined with low PSM ischaemia. BJU Int. 2016; 117:531-6.
rates obtained with our open surgical technique play crit-
ical roles in this high long-term oncological survival. Our 12. Yossepowitch O, Eggener SE, Serio A, et al. Temporary renal
ischemia during nephron sparing surgery is associated with short-
results are consistent with previous studies, and we antic- term but not long-term impairment in renal function. J Urol. 2006;
ipate that our study will add to the successful oncological 176:1339-43.
outcome of OPN studies.
The limitations of our study are retrospective design, a 13. You C, Du Y, Wang H, et al. Laparoscopic Versus Open Partial
small number of patients subjected to PN upon mandato- Nephrectomy: A Systemic Review and Meta-Analysis of Surgical,
ry indications, and inclusion of a single type of surgical Oncological, and Functional Outcomes. Front Oncol. 2020; 10:2261.
method. In addition, more recent studies demonstrate 14. Tachibana H, Kondo T, Yoshida K, et al. Lower incidence of post-
that the amount of remaining kidney tissue post-opera- operative acute kidney injury in robot-assisted partial nephrectomy
tion is the most significant indicator of long-term kidney than in open partial nephrectomy: A propensity score-matched study.
function. The absence of this parameter is the most sig- J Endourol. 2020; 2020; 34:754-762
nificant limitation of our work and will be our field of 15. Lerner SE, Hawkins CA, Blute ML, et al. Disease outcome in
study in the future. patients with low stage renal cell carcinoma treated with nephron
sparing or radical surgery. J Urol. 1996; 155:1868-73.
16. Chang KD, Abdel Raheem A, Kim KH, et al. Functional and
CONCLUSIONS oncological outcomes of open, laparoscopic and robot-assisted partial
This study confirms excellent long-term oncologic and nephrectomy: a multicentre comparative matched-pair analyses with
functional outcomes after OPN in a cohort of patients a median of 5 years’ follow-up. BJU Int. 2018; 122:618-26.
selected from a single institution. We contributed to the
literature by reporting that our patients who underwent 17. Minervini A, Mari A, Borghesi M, et al. The occurrence of intra-
open PN had high oncologic survival, and their kidney operative complications during partial nephrectomy and their impact
on postoperative outcome: results from the RECORd1 project.
functions were well preserved in the long-term follow-up. Minerva Urol Nefrol 2018; 71:47-54
18. Caraballo ER, Palacios DA, Suk-Ouichai C, et al. Open partial
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Correspondence
Efe Bosnali, MD Corresponding Author)
[email protected]
Department of Urology, University of Health Sciences, Derince Training
and Research Hospital, Turkey, 41380

Enes Abdullah Baynal, MD


[email protected]
Naci Burak Çınar, MD
[email protected]
Enes Malik Akdas, MD
[email protected]
Engin Telli, MD
[email protected]
Kerem Teke, MD
[email protected]
Hasan Yılmaz, MD
[email protected]
Özdal Dillioğlugil, MD
[email protected]
Önder Kara, MD
[email protected]
Kocaeli University, School of Medicine, Department of Urology, Kocaeli,
Turkey

Büşra Yaprak Bayrak, MD


[email protected]
Kocaeli University, School of Medicine, Department of Pathology,
Kocaeli, Turkey

Conflict of interest: The authors declare no potential conflict of interest.

Archivio Italiano di Urologia e Andrologia 2023; 95(4):12130

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