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Keywords:

  • partial nephrectomy;
  • renal function;
  • renal scintigraphy;
  • renal tumour

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Study Type – Prognosis (case series)

Level of Evidence 4

What's known on the subject? and What does the study add?

When partial nephrectomy is performed, renal vessels are clamped to avoid bleeding during tumour resection. Renal cooling during renal vessel clamping has the advantage of avoiding renal damage. We consider that the open approach is a choice for avoiding renal damage in patients with a solitary kidney or a risk of chronic kidney disease, if renal cooling cannot be performed in laparoscopic surgery.

The results obtained in the present study suggest that cold ischaemia has the advantage of the recovery of postoperative affected renal function. However, further evaluation for a long period after surgery is needed to evaluate the recovery of affected renal function.

OBJECTIVE

  • • 
    To determine the cause of diminished renal function in the affected kidney after partial nephrectomy (PN) for renal tumour, we analyzed the relationship between operative data and postoperative recovery with respect to renal function.

PATIENTS AND METHODS

  • • 
    From May 2005 to December 2010, pre- and postoperative (1 week and 3 months after the procedure) renal function was evaluated by 99mTc- mercaptoacetyltriglycine clearance in 51 patients treated with open partial nephrectomy (OPN; n= 24) and laparoscopic partial nephrectomy (LPN; n= 27).
  • • 
    LPN was performed via retroperitoneal (RPLPN; n= 14) or transperitoneal (TPLPN; n= 13) routes.
  • • 
    Renal cooling was performed after renal hilar clamping in OPN and RPLPN, although not in TPLPN.

RESULTS

  • • 
    There were 10 patients (two in OPN, six in TPLPN, two in RPLPN) who had diminished renal function in the affected kidney from 1 week to 3 months after PN.
  • • 
    Warm ischaemia (versus cold ischaemia; P= 0.017) during renal hilar clamping resulted in diminished renal function.
  • • 
    Using multivariate analysis, renal cooling influenced postoperative diminished renal function (P= 0.008).

CONCLUSIONS

  • • 
    Successful preservation of renal function after PN depends on renal cooling during renal hilar clamping.
  • • 
    Cold ischaemia for avoiding renal damage is recommended if renal hilar clamping is necessary for tumour extraction.

Abbreviations
eGFR

estimated glomerular filtration rate

LPN

laparoscopic partial nephrectomy

MAG3

mercaptoacetyltriglycine

OPN

open partial nephrectomy

PN

partial nephrectomy

RPLPN

retroperitoneal laparoscopic partial nephrectomy

TPLPN

transperitoneal laparoscopic partial nephrectomy.

INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Partial nephrectomy (PN) for localized renal tumour has an oncological outcome similar to that of radical nephrectomy, which is a significant risk factor for the development of chronic kidney disease [1,2]. Therefore, PN is recommended when aiming to avoid renal dysfunction and is being performed with increased frequency. However, in some patients receiving nephron-sparing surgery, renal function decreased after the procedure. Lane et al. [3] suggested that lower preoperative GFR, solitary kidney, older age, gender, tumour size and longer ischaemic interval all predicted lower GFR after PN.

Previous studies have shown that serum creatinine and GFR did not significantly change compared to the preoperative data when the resection was performed in patients with a normal contralateral kidney [4,5]. These studies suggested that renal function in the affected kidney as estimated by renal scintigraphy is less influenced by extrarenal factors and that scintigraphy is an appropriate method for evaluating renal function [4]. We have shown that some patients had a decrease of renal function in the affected kidney after PN, despite having no significant change in total renal function [5].

In the present study, aiming to determine the factors predicting diminished renal function in the affected kidney, we evaluated pre- and postoperative renal function related to PN using 99mTc-mercaptoacetyltriglycine (MAG3) and analyzed the correlation between patient characteristics and operative data, as well as renal function in the affected kidney.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

From May 2005 to February 2010, 51 patients were diagnosed with renal tumours, including 37 (73%) men and 14 (27%) women, with a median age of 58 years (range, 26–79 years). Patients were treated with open PN (OPN; n= 24) or laparoscopic PN (LPN; n= 27), including transperitoneal LPN (TPLPN; n= 13) or retroperitoneal LPN (RPLPN; n= 14), in a single institution. Patients provided their consent with respect to an evaluation of renal function by renal scintigraphy after the operation.

In cases of OPN or RPLPN, the affected kidney was cooled by ice slush or near-freezing saline, respectively, after clamping of the renal vessels. In cases of RPLPN, near-freezing saline was infused from the stopcock of a port that was connected to a pressurized infusion bag using a wide irrigation tube. Near-freezing saline (2 L) could be rapidly injected at the same time as aspirating the saline that was warmed in the retroperitoneal space [6]. For preparation of near-freezing saline, a 1-L bag of saline was placed in a freezer at −30 °C for 3 h before surgery, and subsequently kept in a refrigerator at 4 °C. This protocol resulted in ice formation in almost half of the bag. The saline temperature was 2.0–4.0 °C. To prevent renal damage, i.v. injections of 100 mL of 20% mannitol were administered before renal artery clamping and after removal of the clamp in all cases.

Renal function was analyzed after the operation and 1 week and 3 months after the operation by estimated GFR (eGFR) using the equation: 194× serum creatinine−1.094× age−0.287× (1 − sex × 0.261), where sex was 0 for males and 1 for females, and renal scintigraphy using 99mTc-MAG3. Renal function in the affected kidney was evaluated by the ratio of affected renal MAG3 clearance to contralateral renal MAG3 clearance. The differences were evaluated by the Mann–Whitney U-test, Fisher's test and the chi-squared test for univariate analysis, as well as by logistic regression analysis for multivariate analysis.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Preoperative and postoperative renal function in the affected kidney after surgery is shown in Fig. 1. The affected renal function, as evaluated by the affected/contralateral renal MAG3 clearance ratio, decreased by ≈40% at 1 week after surgery in 41 patients (Fig. 1A), and then recovered by ≈10% from 1 week to 3 months after surgery, although not in 10 patients (two in OPN, six in TPLPN, two in RPLPN ) (Fig. 1B).

image

Figure 1. Preoperative (Pre-op) and postoperative affected kidney function estimated by renal scintigraphy using 99mTc- mercaptoacetyltriglycine (MAG3). The percentage was determined by the ratio of affected/contralateral renal MAG3 clearance. A, Affected renal function decreased by ≈40% at 1 week after surgery in 41 patients, and then recovered by ≈10% from 1 week to 3 months after surgery. B, The affected renal function continuously decreased from 1 week to 3 months after surgery in 10 patients.

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Patient characteristics and operative data in patients with recovered and continuously decreased renal function in the affected kidney after surgery are shown in Tables 1 and 2. There were no differences in the patient characteristics, median tumour size, median operating time, median ischaemic time and median blood loss between the groups. Intra-operative complications were observed in one patient in the recovered group who experienced pneumothorax during LPN. Postoperative haematoma (no blood transfusion) was observed in one patient treated with OPN in the recovered group and in one patient treated with LPN in the decreased renal function group. Pathological examination showed renal cell carcinoma in 44 patients, angiomyolipoma in four patients and oncocytoma in three patients. All surgical margins were found to be negative for residual malignancy (data not shown).

Table 1.  Patient characteristics
VariableRecoveredDecreasedTotal P
Patients (n)411051 
Side (n)    
 Left163190.869
 Right25732
Sex (n)    
 Male316370.551
 Female10414
Age (years), mean (range)58 (26–79)57 (38–79)58 (26–79)0.906
Hypertension (n)151160.054
Diabetes mellitus (n)7070.320
Preoperative creatinine (mg/dL), mean (range)0.77 (0.42–1.24)0.72 (0.49–1.06)0.77 (0.42–1.24)0.822
Preoperative estimated glomerular filtration rate (mL/min/1.73 m2), mean (range)75.7 (44.6–146.5)74.5 (51.9–105.8)75.7 (44.6–146.5)0.831
Table 2.  Operative data
VariableRecoveredDecreasedTotal P
Operation (n)    
 Open partial nephrectomy222240.119
 Laparoscropic partial nephrectomy19827
Tumour size (cm), median (range)2.5 (1.0–4.2)2.3 (1.2–3.5)2.5 (1.0–4.2)0.279
Operating time (min), median (range)192 (118–435)226 (123–345)192 (118–435)0.313
Ischaemic time (min), median (range)31 (14–79)38 (18–64)33 (14–79)0.419
Ischaemic (n)   
 <30 min202220.196
 >30 min21829
 Cold344380.017
 Warm7613
Blood loss (mL), median (range)150 (16–800)175 (20–1000)150 (16–1000)0.731

The number of patients receiving cold ischaemia during hilar clamping in the recovered group (34/41) was significantly more than that in the decreased group (4/10) (P= 0.017). In 29 patients with an ischaemic time >30 min, 21 (72.4%) patients had recovered affected renal function from 1 week to 3 months after PN. In eight patients with decreased renal function after an ischaemic time >30 min, five patients received renal hilar clamping with warm ischaemia (Table 2 and data not shown). The results of logistic regression analysis showed that only cold ischaemia was predictive of recovered affected renal function after PN (P= 0.008) (Table 3). All other evaluated factors did not correlate with postoperative decreased renal function.

Table 3.  Logistic regression analysis of improved renal function in the affected kidney
 Odds ratio P 95% CI
Male sex8.8200.0630.89–87.48
Ischaemia20.7660.0082.20–196.34

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Because the therapeutic outcome of PN is not inferior to that of radical nephrectomy, nephron-sparing surgery is recommended for small renal tumours. However, the decrease in renal function after PN is unavoidable because normal tissue is excised during tumour resection and the affected kidney is damaged as a result of the procedure.

It is difficult to evaluate postoperative affected renal function by serum creatinine or eGFR because of the influence of the normal contralateral kidney. For some patients in the present study, the levels of serum creatinine and eGFR were not affected by the procedure, despite a decrease in affected renal function as evaluated by MAG3 clearance. Studies have reported data on affected renal function after PN in a solitary kidney. Lane et al. [7] reported that a longer warm ischaemic time and preoperative GFR were associated with poorer postoperative GFR in patients receiving LPN with warm ischaemia during hilar clamping. Wszolek et al. [8] showed that non-ischaemic OPN was associated with superior preservation of GFR compared to ischaemic OPN. Shekarriz et al. [9] evaluated affected renal function with pre- and postoperative renal scans. In patients receiving LPN with a warm ischaemic time >30 min, affected renal function was decreased at 3 months after the procedure [9]. In the present study, we evaluated affected renal function by renal scintigraphy in patients receiving OPN and LPN with cold and warm ischaemia. We found that 19.6% (10/51) of patients have decreased renal function in the affected kidney from 1 week to 3 months after PN. However, in 29 patients with an ischaemic time >30 min, 21 (72.4%) patients recovered function in the affected kidney after PN.

The renal vessels are usually clamped to avoid bleeding when the tumour is extracted by PN. The renal hilum is clamped with renal cooling (cold ischaemia) in many cases because cooling avoids severe damage to the kidney. By contrast, warm ischaemia refers to the clamping of blood vessels without cooling the kidney, and a short ischaemic time is important for the prevention of renal dysfunction if this method is used. A long warm ischaemic time is associated with a poor recovery of renal function and an increased risk of renal dysfunction [4,10–13]. The safe limit for warm ischaemic time has been discussed in recent studies showing renal dysfunction in the 35–50-min range [7,11,14–16]. Previous studies have reported methods for reducing warm ischaemia, such as the modified closure technique [17], and on-demand extracorporeal clamping [18]. Wszolek et al. [8] reported that the technique of non-ischaemic PN accounts for a better preservation of renal function. In the present study, all patients received hilar clamping during tumour resection and it was found that renal cooling affects postoperative recovery of renal function in the affected kidney. A previous study also suggested that a warm ischaemic time >30 min influenced the postoperative recovery of renal function [5]. Renal cooling for avoiding renal damage should be performed if renal hilar clamping is necessary for tumour extraction.

For the cases of LPN in the present study, ischaemic time in RPLPN was longer than with TPLPN as a result of renal cooling during hilar clamping in RPLPN. However, six of 13 patients with TPLPN had decreased renal function in the affected kidney from 1 week to 3 months after PN, whereas 12 of 14 patients with RPLPN had recovered renal function in the affected kidney. For cold ischaemia in RPLPN, we performed an injection of near-freezing saline from the stopcock of the port that was connected to a pressurized infusion bag using a wide irrigation tube. This method provides efficient renal cooling because cold saline can be rapidly injected at the same time as aspirating the saline that has been warmed in the retroperitoneal space. Although the ischaemic time was >30 min, including the renal cooling time in 13 of 14 patients receiving RPLPN, only two patients had decreased renal function in the affected kidney from 1 week to 3 months after surgery. A single patient in the recovered group received RPLPN even with 79 min of renal hilar clamping. The affected renal function decreased by 63% at 1 week after surgery, and then recovered by 27% from 1 week to 3 months. The serum creatinine and eGFR after the procedure did not change compared to preoperative values (Table 2 and data not shown). Although further evaluation for a long period after surgery is needed to evaluate the recovery of affected renal function, these results suggest that a long ischaemic time with renal cooling was compatible with renal function preservation after PN.

Cold ischaemia has the advantage of the recovery of postoperative affected renal function. However, in some cases of LPN, the transperitoneal approach was necessary as a result of the location of the tumour and warm ischaemia was performed during tumour dissection. We consider that the open approach is a choice for avoiding renal damage in patients with a solitary kidney or a risk of chronic kidney disease, if renal cooling cannot be performed in LPN. Cold ischaemia for avoiding renal damage is expected to be better than warm ischaemia during renal hilar clamping.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES