Trends in the operative management of renal tumours over a 14-year period

Authors

  • Sompol Permpongkosol,

    1. Department of Urology, Johns Hopkins Medical Institutions, Baltimore, MD and The Institute for Urology, North Shore-LIJ Health System, Long Island, New York, NY, USA
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  • Herman S. Bagga,

    1. Department of Urology, Johns Hopkins Medical Institutions, Baltimore, MD and The Institute for Urology, North Shore-LIJ Health System, Long Island, New York, NY, USA
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  • Frederico R. Romero,

    1. Department of Urology, Johns Hopkins Medical Institutions, Baltimore, MD and The Institute for Urology, North Shore-LIJ Health System, Long Island, New York, NY, USA
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  • Stephen B. Solomon,

    1. Department of Urology, Johns Hopkins Medical Institutions, Baltimore, MD and The Institute for Urology, North Shore-LIJ Health System, Long Island, New York, NY, USA
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  • Louis R. Kavoussi

    Corresponding author
    1. Department of Urology, Johns Hopkins Medical Institutions, Baltimore, MD and The Institute for Urology, North Shore-LIJ Health System, Long Island, New York, NY, USA
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The Institute for Urology, North Shore-LIJ Health System, 300 Community drive, 9 Tower, Manhasset, NY 11030, USA. e-mail: kavoussi@nshs.edu

Abstract

OBJECTIVE

To review the trends in the operative management of renal tumours over a 14-year period at a university hospital, as the therapeutic options available for treating renal tumours have increased over the past decade.

PATIENTS AND METHODS

The study was a retrospective chart review of 1621 consecutive patients undergoing treatment for renal tumours from January 1991 to March 2005. The characteristics assessed included patient demographics, tumour size, operative duration and treatment.

RESULTS

During the study period, 624 (38.6%) open, 883 (54.6%) laparoscopic and 111 (6.7%) percutaneous approaches were performed. The number of renal tumours treated increased annually, as did the use of minimally invasive techniques (93.4% in 2005). Conversely, the number of open surgical treatments used declined both absolutely and proportionally. Over the study period, for tumours of ≤ 4 cm, laparoscopic partial nephrectomy was the most common approach (41.0%). Percutaneous ablation has also made an impact as a treatment method for small tumours (13.8% in 2005). For tumours of >7 cm, open radical nephrectomy (ORN) was the most common method of treatment over all years. However, since 2002, laparoscopic radical nephrectomy (LRN) surgery has been increasingly used over ORN for treating this tumour group (73% LRN vs 19.2% ORN in 2004).

CONCLUSION

The available treatment options for renal tumours have increased significantly since the early 1990s. At a university hospital in which there are physicians with a specific interest in minimally invasive surgery and ablative treatments, minimally invasive approaches have become the standard treatment.

Abbreviations
(O)(L)PN

(open) (laparoscopic) partial nephrectomy

(O)(L)RN

(open) (laparoscopic) radical nephrectomy

(O)(P)(L)RC

(open) (percutaneous) (laparoscopic) renal cryoablation

(P)(L)RF

(percutaneous) (laparoscopic) renal radiofrequency ablation.

INTRODUCTION

Since the early 1990s surgical options for managing renal tumours have markedly increased. Traditionally, open radical nephrectomy (ORN) was the only method to manage renal tumours [1]. Subsequently open partial nephrectomy (OPN) was explored as a method to preserve renal function. Initial applications of nephron-sparing surgery in the modern era were limited to imperative indications such as bilateral renal masses or a tumour in a functionally or anatomically solitary kidney. Advances in renal imaging and clinical staging have led to the increased detection of incidental and small tumours amenable to local excision.

The novel minimally invasive approach for treating renal masses began in 1991 when Clayman et al.[2] performed the first laparoscopic radical nephrectomy (LRN) for a tumour-bearing kidney. This subsequently paved the way for investigators to study a variety of approaches including laparoscopic partial nephrectomy (LPN), laparoscopic ablative surgery, and percutaneous needle ablative procedures [3–5]. Several studies showed that small renal masses could be effectively treated with low peri-operative morbidity, when performed by an experienced laparoscopic surgeon [6].

Despite the benefits of minimally invasive renal surgery, actual practice patterns for management of renal tumour vary widely. Recently, reports from community urology practices have assessed the incorporation of LN into general practice [7,8]. The diffusion of practice patterns in an academic medical centre has been less well defined, and studies that systematically examined the operative management of renal tumours at university hospitals are lacking. In this report we evaluate the trend in operative management of renal tumours at a large academic medical centre, where both skilled laparoscopic and open surgeons practice urology. The objective of this study was to characterize the variation in surgical management of renal tumours in a university hospital over a 14-year period.

PATIENTS AND METHODS

After approval by the Institution Review Board, the records for patients who were treated for a renal mass between January 1991 and March 2005 were evaluated retrospectively for patient demographics, pathological results and operative duration. The data were obtained from the renal surgical database of the institution. Patients with bilateral or multiple procedures, kidney transplantation, or who were children, were excluded from the analysis. The mean operative duration was based on the time between the patients’ entry and exit from the operating room.

Renal mass size was determined on the basis of clinical staging. Treatment was one of nine types: ORN, OPN, open renal cryoablation (ORC), LRN, LPN, laparoscopic renal radiofrequency ablation (LRF), laparoscopic renal cryoablation (LRC), percutaneous renal radiofrequency ablation (PRF), and percutaneous renal cryoablation (PRC).

RESULTS

In all, 1652 renal tumours were treated in 1621 patients at our institution. Of these, 624 (38.6%) surgical procedures were via the traditional open approach, 883 (54.6%) laparoscopically and 111 (6.7%) percutaneously. The indications for treatment were tumours or lesions suspicious for malignancy. Table 1 shows the clinical characteristics of the patient’s demographics and preoperative tumour characteristic of each group; 65% of the patients were men, and there was no difference in practice patterns for gender. The mean (sd) age of patients who were treated was 59.5 (13.1) years. Patients treated with renal ablation were older than those who had excisional surgery. The American Society of Anesthesiologists classification (ASA) score 3 was 57.9% for OPN, 66.7% for ORC, 57.8% for LPN, 100% for LRF, 56.7% for LRC, 60.3% for PRF and 58.3% for PRC. The comorbidity rate associated with open, laparoscopic and percutaneous approaches was 49.9%, 57.2% and 95.5%, respectively. The mean (range) preoperative serum creatinine level was 1.4 (1.3–1.7) mg/dL. The mean (sd) renal mass size was 4.8 (3.6) cm, and the mean renal mass sizes were <3 cm in all groups except the ORN (7.2 cm), OPN (3.6 cm) and LRN (5.5 cm) groups (Table 1).

Table 1.  The patients’ and renal tumour characteristics of each group treated between January 1991 and March 2005
VariableORNOPNORCLRNLPNLRFLRCPRFPRCTotal
Patients, n (%)444 (27)178 (11)  6 (0.4)516 (31.8)333 (20.5)  3 (0.2) 30 (1.9)63 (3.9)48 (3.0) 1621
Mean (sd) age, years 59.3 (12.8) 57.7 (13.4) 73.3 (16.0) 59.6 (12.7) 59.5 (13.1) 49.7 (17.9) 64.2 (12.8)63.5 (18)67.4 (13.8)  59.5 (13.1)
Men/women281/163 112/66  1/5340/176204/129  3/0 16/1445/1836/12 
ASA score, n (%)
 1 14 (3)  8 (2)  6 (2)  0 0 0 
 2180 (41) 70 (39)  2229 (44)134 (40) 12 (40)24 (38)18 (38) 
 3217 (49)103 (58)  4250 (49)189 (58)  3 17 (57)38 (60)28 (58) 
 4 33 (7)  5 (3)_ 29 (6)  4 (1)  1 (3) 1 (2) 2 (4) 
Comorbidity, n (%)216 (49) 94 (53)  3290 (57)188 (57)  1 24 (80)60 (95)46 (96) 
Mean CR level, mg/dL  1.5  1.3  1.4  1.7  1.1  1.0  1.2 1.7 1.6 
Tumour
 mean (sd) size, cm  7.2 (4.2)  3.6 (2.0)  2.5 (1.7)  5.5 (3.5)  2.8 (1.8)  2.4 (0.4)  2.8 (1.4) 2.2 (0.7) 2.3 (1.0)   4.8    (3.6)
 right/left, n220/224 98/85  4/2266/250182/151  0/3 15/1529/3422/26 
Mean (sd) OR, min242.2 (98.6)261.1 (66.7)137.0 (87.7)228.0 (82.8)205.7 (75.7)203.3 (24.4)167.1 (71.8)67.6 (24.6)80.5 (22.6) 
Pathology, n
Benign 59 42  3 81104  2  8 7 3 309   (19.1)
 Oncocytoma 24 14  3 34 36  0 5 1 
 AML  11 10 12 34  1  3 2 2 
 cyst  2  5  4 20  5 0 0 
 other 22 13 31 14  1  0 0 0 
Malignant385136  3435229  1 1940361284 (79.2)
 RCC369 131  1428223  1 193935 
  Clear cell201 85  2291130  1 131526 
  Papillary 39 32 86 59  2 7 6 
  Chromophobe 13  0 28 20  0 0 0 
  Granular cell  1  0  0 0 1 
  Mixed 14  9  9  7  0 0 2 
  Non-specific 101  5 14  7  417 0 
 Other 16  5  7  6 1 1 
No diagnosis  0  0  316 9  28   (1.7)

The mean (sd) operative time (OR) of all procedures was 227.3 (88) min. The mean procedure time was <90 min in the PRF and PRC groups, 90–180 min in the ORC and LRC groups, 180–240 min in the LRF, LPN and LRN groups, and >240 min in the ORN and OPN groups (Table 1). The number of patients with renal tumours who had operative management increased by a factor of eight, from 34 cases in 1991 to 271 cases in 2004 (Fig. 1). The number of minimally invasive operations (laparoscopic and percutaneous procedures) also increased significantly over time, while the number of open surgical procedures decreased (Fig. 2). It was 3 years from the first published report until LRN, LPN and LRC were established at our institution. This corresponded with recruitment of a surgeon with laparoscopic skills to the hospital. For the percutaneous ablation, it was 1 and 8 years after the first report before the first case of PRF and PRC, respectively, was performed at our institution. In 1991, the treatment of renal tumours was with open surgery in all cases, but by March 2005 only 6.6% were treated with open surgery and LRN was the most common treatment, in 31.7% of patients (Fig. 3). Also, LRN was performed in 9.3% of patients (five/54) in 1994 and became the major treatment approach in 2000 (55.4%). From 2001 to 2005 the percentage of LRN decreased annually to 34.3% (93/271). This corresponded with the introduction of LPN and percutaneous ablative techniques. LPN increased from 3% in 1996 to the majority (41%) of total tumour operations in 2005. By contrast, LRN procedures that year decreased to second in frequency (37.7%). Percutaneous ablation increased from 2.5% to 13.7% from 2000 to 2004, and was the third most common procedure in 2005. Conversely, the number of ORN decreased from 76.5% in 1991 to 4.1% in 2004. Figure 4 shows, by renal mass size, the number of renal tumours treated from 1991 to March 2005. There was a significant increase every year in the number of small renal masses (≤4 cm), from seven tumours in 1991 to 184 in 2004; 26.3 times as many in 2004 as in 1991. Figure 5 shows the distribution of procedures according to renal mass size. Patients with masses of ≤ 4 cm were treated with the widest variety of approaches. LPN was the most common procedure (31.7%), followed by LRN (26.6%), OPN (14.7%) and percutaneous ablation (13.6%). Most tumours of 4–7 cm were treated with LRN (41.9%) and ORN (38.3%), and tumours of >7 cm were managed with ORN (61.8%) and LRN (34.6%), respectively. However, since 2002, LRN surgery has been increasingly dominant over ORN for treating this tumour group (73% LRN vs 19.2% ORN in 2004).

Figure 1.

The operative management of renal tumours from 1991 to March 2005. LRA, laparoscopic renal ablation; PRA, percutaneous renal ablation.

Figure 2.

The percentage of renal tumours managed with minimally invasive surgery (laparoscopic and percutaneous approaches) compared to open surgery, 1991–2005.

Figure 3.

The percentage trends in operative management of patients with renal tumour in a medical school; 1991–2005. LRA, laparoscopic renal ablation; PRA, percutaneous renal ablation.

Figure 4.

The tumour sizes according to year, 1991–2005.

Figure 5.

The distribution of the procedure according to the size of the renal mass from 1991–2005. LRA, laparoscopic renal ablation; PRA, percutaneous renal ablation.

DISCUSSION

During the latter half of the 20th century, great strides were made in the management of renal tumours. Improvements in radiological imaging led to earlier diagnosis and improved staging. Refinements in surgical techniques, and enhanced understanding of the immunobiology of solid tumours, have led to an improved outlook for patients with RCC [9]. Several innovations during the 1990s brought about a major reshaping of the operative management of RCC. Minimally invasive surgical techniques were developed that produced equivalent outcomes when compared to traditional open surgery. Initial studies assessed the efficacy of minimally invasive surgery for RCC. The 5- and 10-year disease-free and patient survival rates are equivalent for LRN and ORN [10]. The preliminary oncological outcomes of LPN are also paralleling those for open approaches [11]. The results of LRC and PRF of renal masses also appear promising in selected patients [5,12].

The introduction of minimally invasive techniques has resulted in an evolution in the operative management of renal tumours (Fig. 1); several factors are driving this trend. First, there is societal desire for less-invasive approaches. Patients understand the need to cure cancer, but also are aware of advances in surgery and demand approaches that address secondary issues such as pain and convalescence. Moreover, the advent of the Internet and broad bandwidth media coverage is educating patients about available options. Also facilitating the introduction of these approaches is the greater incidence of smaller renal tumours through the liberal use of novel radiographic imaging techniques [9]. Application of these new management options can be assessed in small tumours where the risk of under-treatment does not necessarily negate subsequent traditional treatment.

Over time the operative management of renal tumours at our institution has changed significantly. The mean time for implementation of a new procedure was 3 years from the first published report, excluding PRC. In addition, each technique had its history of development related to technology, ‘clinical champions’ and available data. It took 6 and 9 years for LRN and LPN, respectively, to become a standard treatment at a relatively progressive university hospital. The primary driver for initial adoption was the availability of a ‘clinical champion’ who assessed the technology. Over time, a clinician focused and dedicated to minimally invasive surgery introduced other faculty members to the technology and provided a framework for propagation. At our institution incorporation was directly related to the recruitment and support of ‘clinical champions’ with each successive technology.

The conventional curative therapy for renal tumours at our institution has become the laparoscopic approach, with a progression from complete to partial nephrectomy. Patients who had renal tumours of <4 cm were more likely to be treated with LPN, from 3% to 33.3%. This migration has paralleled a decrease in the mean size of the renal tumours detected and an increase in organ-confined tumours from 1991 to 2004 [13]. LPN is a technically challenging procedure which can explain the lag time for introduction. This delay has also been noted in community hospitals [7,8].

The renal ablative procedures are the newest therapeutic option. These are less invasive than surgical therapy and the potential exists to perform these under local anaesthesia in an outpatient setting [14]. The primary deterrents to widespread acceptance include absence of long-term oncological outcomes, lack of familiarity with technology, delay in generation of Current Procedural Terminology billing codes, and in the case of image-guided procedures, lack of collaboration with radiology. There are no long-term follow-up studies or comparative data providing a way to compare effectiveness of these different approaches. In 2000, our institution reported on seven patients treated with both ORC and LRC, with no reported local recurrence [15]. While far more invasive than a percutaneous approach, it has several potential benefits; the ability to see the margins of the ice-ball, the ability to displace and protect adjacent structures, and the ability to potentially control bleeding [16]. The series by Gill et al.[12] of LRC recently provided 3-year oncological outcome data in 51 patients undergoing cryotherapy for a unilateral, sporadic renal tumour; the 3-year cancer-specific survival was 98%. As such, the oncological efficacy documented by these laparoscopic results is fundamentally responsible for the greater acceptance of renal cryotherapy in general, and have fuelled increased interest in the even less-invasive percutaneous approaches. Results for small tumours are promising, but the short-term oncological outcome of PRF showed lower oncological control in tumours of >3.0 cm and for central lesions [5].

In conclusion, the incorporation of new techniques into the daily routine of a university practice is a gradual process that is affected by many variables. The development of laparoscopic and ablative techniques is changing the approach to renal masses, and minimally invasive surgery has developed as a standard treatment option for many patients with renal masses in a university setting.

ACKNOWLEDGEMENTS

The authors thank Carolyn Schum M.A. as well as Sahar Kohanim, Soroush Rais-Bahrami, Guilherme Lima and Niwat and Suparak Aranyakasemsuk for their assistance in preparing our manuscript.

CONFLICT OF INTEREST

None declared.

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