VOLUME

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2014

JOURNAL OF CLINICAL ONCOLOGY

O R I G I N A L

R E P O R T

Comparative Effectiveness of Robot-Assisted and Open Radical Prostatectomy in the Postdissemination Era Giorgio Gandaglia, Jesse D. Sammon, Steven L. Chang, Toni K. Choueiri, Jim C. Hu, Pierre I. Karakiewicz, Adam S. Kibel, Simon P. Kim, Ramdev Konijeti, Francesco Montorsi, Paul L. Nguyen, Shyam Sukumar, Mani Menon, Maxine Sun, and Quoc-Dien Trinh See accompanying editorial on page 1394 Giorgio Gandaglia, Pierre I. Karakiewicz, and Maxine Sun, Cancer Prognostics and Health Outcomes Unit, University of Montreal Health Center, Montreal, Quebec, Canada; Giorgio Gandaglia and Francesco Montorsi, Urological Research Institute, Vita-Salute San Raffaele University, Milan, Italy; Jesse D. Sammon and Mani Menon, Vattikuti Urology Institute, Henry Ford Health System, Detroit, MI; Steven L. Chang, Toni K. Choueiri, Adam S. Kibel, Ramdev Konijeti, Paul L. Nguyen, and Quoc-Dien Trinh, Dana-Farber Cancer Institute, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA; Jim C. Hu, David Geffen School of Medicine at University of California, Los Angeles, Los Angeles, CA; Simon P. Kim, Yale University, New Haven, CT; and Shyam Sukumar, University of Minnesota, Minneapolis, MN. Published online ahead of print at www.jco.org on April 14, 2014. Both G.G. and J.D.S. contributed equally to this work. Terms in blue are defined in the glossary, found at the end of this article and online at www.jco.org. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article. Corresponding author: Quoc-Dien Trinh, MD, Division of Urologic Surgery, 45 Francis St, ASB II-3, Boston, MA 02115; e-mail: [email protected]. © 2014 by American Society of Clinical Oncology 0732-183X/14/3214w-1419w/$20.00 DOI: 10.1200/JCO.2013.53.5096

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Purpose Given the lack of randomized trials comparing robot-assisted radical prostatectomy (RARP) and open radical prostatectomy (ORP), we sought to re-examine the outcomes of these techniques using a cohort of patients treated in the postdissemination era. Patients and Methods Overall, data from 5,915 patients with prostate cancer treated with RARP or ORP within the SEER-Medicare linked database diagnosed between October 2008 and December 2009 were abstracted. Postoperative complications, blood transfusions, prolonged length of stay (pLOS), readmission, additional cancer therapies, and costs of care within the first year after surgery were compared between the two surgical approaches. To decrease the effect of unmeasured confounders, instrumental variable analysis was performed. Multivariable logistic regression analyses were then performed. Results Overall, 2,439 patients (41.2%) and 3,476 patients (58.8%) underwent ORP and RARP, respectively. In multivariable analyses, patients undergoing RARP had similar odds of overall complications, readmission, and additional cancer therapies compared with patients undergoing ORP. However, RARP was associated with a higher probability of experiencing 30- and 90-day genitourinary and miscellaneous medical complications (all P ⱕ .02). Additionally, RARP led to a lower risk of experiencing blood transfusion and of having a pLOS (all P ⬍ .001). Finally, first-year reimbursements were greater for patients undergoing RARP compared with ORP (P ⬍ .001). Conclusion RARP and ORP have comparable rates of complications and additional cancer therapies, even in the postdissemination era. Although RARP was associated with lower risk of blood transfusions and a slightly shorter length of stay, these benefits do not translate to a decrease in expenditures. J Clin Oncol 32:1419-1426. © 2014 by American Society of Clinical Oncology

INTRODUCTION

Originally described in the 1950s and subsequently popularized by Walsh in the 1980s, radical retropubic prostatectomy (RP) has long been established as a standard first-line treatment modality for clinically localized prostate cancer (PCa).1 Although open RP (ORP) represented the standard surgical approach for many years, minimally invasive approaches, mainly robot-assisted RP (RARP), have been widely adopted in the United States over the last decade. As of 2009, more than 60% of all RPs performed in the United States have been done robotically.2 Although single-institution studies have shown benefits of RARP over ORP,3 the widespread dissemination of RARP has been in part attributed to extensive

patient-directed marketing and increasing hospital market competition. Furthermore, large observational studies, such as the landmark article by Hu et al,4 showed no difference between RARP and ORP with regard to postoperative complications and long-term functional outcomes. When considering that RARP is associated with excess spending of at least $4 million per year at the national level,5,6 many have questioned the value of costly technology in the absence of strong evidence demonstrating its superiority.7 Nonetheless, it is important to consider that many of these initial studies were performed during the early robotic era and may no longer be applicable in contemporary patients.8,9 Because the technology was widely adopted in the latter part of the © 2014 by American Society of Clinical Oncology

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1419

Gandaglia et al

last decade, studies originating from earlier years may not offer a valid assessment of contemporary RARP outcomes.4 Given these considerations, we sought to re-examine the outcomes of RARP versus ORP, using a cohort of patients undergoing surgery for PCa from an era when RARP has supplanted ORP as the main surgical approach for PCa. We hypothesized that, in a cohort of patients treated after the period of broad RARP diffusion, the minimally invasive approach would be associated with lower rates of postoperative complications, blood transfusions, and prolonged length of hospital stay compared with ORP. PATIENTS AND METHODS Population Sources The current study relied on the most recent version of the SEERMedicare insurance program linked database. The SEER registries cover approximately 28% of the US population with Medicare administrative data. Medicare insurance includes approximately 97% of Americans age ⱖ 65 years. Linkage to the SEER database is complete for approximately 93% of patients.10 To determine whether the population identified in SEER-Medicare is representative of the entire US population under Medicare coverage, we relied on the Nationwide Inpatient Sample (NIS) to examine the utilization of RARP versus ORP at the national level. The NIS is an all-payer database that is a 20% stratified probability sample of US hospitals, which allows for nationally representative population-level estimates of available data fields. Study Population Overall, 6,310 patients with histologically confirmed PCa (International Classification of Diseases [ICD] for Oncology site code 61.9, histologic code 8140) age 65 years or older and treated with RP from October 2008 to December 2009 were identified from the SEER-Medicare database. This time frame was selected because a specific modifier code for the robotic-assisted approach was introduced on October 1, 2008 (ICD-9, Clinical Modification procedure code 17.42), which allowed for accurate identification of RARP. Patients who underwent ORP were also abstracted. Exclusion criteria consisted of age more than 80 years (n ⫽ 97), metastatic disease (n ⫽ 26), unknown tumor stage (n ⫽ 130), unknown tumor grade (n ⫽ 123), and unknown pelvic lymph node dissection (PLND) status (n ⫽ 19). This resulted in 5,915 assessable patients. Covariates For each patient, age at diagnosis, year of diagnosis, race, population density, marital status, 2000 census tract percentage with 4-year college edu-

A

cation, 2000 census tract annual median income, region, Gleason score, preoperative prostate-specific antigen, clinical and pathologic stage, PLND status, and nodal stage were assigned using the SEER data. The Charlson comorbidity index (CCI) was derived from the Medicare claims 1 year before PCa diagnosis and categorized as 0, 1, 2, and ⱖ 3 using a previously validated algorithm.11 Finally, patients were stratified into three risk groups (low v intermediate v high) based on the D’Amico risk classification.12 Outcomes Postoperative complications and blood transfusions that occurred within 30 and 90 days after surgery were recorded. Similar to previous methodologies,4 the following seven schemes of postoperative complications were assessed using the ICD-9 and Current Procedural Terminology codes (Appendix Table A1, online only): cardiac, respiratory, genitourinary, vascular, wound, and miscellaneous (medical and surgical). Prolonged length of stay (pLOS) was defined as a hospitalization beyond the median (⬎ 2 days) after surgery. Additionally, we focused on 30- and 90-day readmission rates after surgery as determined by any hospitalization within 30 and 90 days of the index discharge date.13 An additional outcome consisted of the administration of additional cancer therapies (ie, radiotherapy and androgen-deprivation therapy).4 In particular, we evaluated the administration of postoperative therapies within 6 months from surgery (adjuvant treatments)14 and at the last follow-up. Finally, to determine RP costs, we summed all Medicare health care expenditures from inpatient, outpatient, and physician services within 12 months from surgery. Using each patient as his own control, we subtracted health expenditures accrued in the 12 months before surgery (baseline annual health care charges), as previously reported.15 All expenditures are reported in 2009 US dollars. Statistical Analyses Temporal trends of the rates of robotic utilization were assessed by examination of the NIS and quantified using linear regression to establish the estimated monthly percent change (EMPC). Trends in robotic utilization were examined in the overall US population and in patients older than age 65 years (Medicare eligible). All comparative analyses were based on the SEER-Medicare cohort, using a two-step instrumental variable analysis to reduce residual confounding as a result of unmeasured patient and/or other pertinent biases.16 The instrument variable used was the local area treatment pattern for RARP. The instrument was created by grouping patients from the SEER-Medicare database according to hospital referral regions, as developed by the Dartmouth Atlas of Health Care.17 This was calculated as the proportion of patients who received RARP in each health service area (HSA). In the event that some HSAs had

B 100

Percentage of Medicare-Elligible Men

80 Open 60 Robotic 40

20

P .001

Robotic use

EMPC 1.70%

95% CI 1.3 to 2.1

80 Open 60 Robotic 40

20

95% CI 0.7 to 2.4

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Robotic use

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Percentage of Men

100

Fig 1. Temporal trends of robotic use in men undergoing radical prostatectomy between October 2008 and December 2009 included in the Nationwide Inpatient Sample (A) overall and (B) including only Medicare-eligible patients. EMPC, estimated monthly percent change. 1420

© 2014 by American Society of Clinical Oncology

JOURNAL OF CLINICAL ONCOLOGY

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Effectiveness of Robot-Assisted Radical Prostatectomy

Table 1. Demographics and Clinical Characteristics of Patients Treated for Nonmetastatic Prostate Cancer Between October 2008 and December 2009 Within the SEER-Medicare Database Stratified According to the Surgical Approach (ORP v RARP) Demographic or Clinical Characteristic Total patients Age at diagnosis, years Mean Median IQR Year of diagnosis 2008 2009 Race White African American Other Marital status Married Unmarried Population density Metropolitan Nonmetropolitan Annual median income, US dollars ⱕ $38,012 $38,013-$50,954 $50,955-$69,389 ⱖ $69,390 College education, % of patients ⱕ 14.3 14.4-25.4 25.5-42.2 ⱖ 42.3 CCI 0 1 2 ⱖ3 Clinical stage ⱕ T2a T2b ⱖ T2c Gleason score ⱕ6 7 8-10 Preoperative PSA, ng/mL ⱕ 10 10-20 ⬎ 20 Unknown Risk group Low Intermediate High PLND status PLND not performed PLND performed Pathologic stage T2 T3 T4 Unknown

Total No. of Patients 5,915

ORP % 100

RARP

No. of Patients

%

No. of Patients

%

2,439

41.2

3,476

58.8

P .01

69.1 68.0 66.0-71.0

69.2 69.0 67.0-71.0

69.0 68.0 66.0-71.0 .1

1,217 4,698

20.6 79.4

527 1,912

21.6 78.4

690 2,786

19.9 80.1

4,869 530 516

82.3 9.0 8.7

1,996 235 208

81.8 9.6 8.5

2,873 295 308

82.7 8.5 8.9

4,606 1,309

77.9 22.1

1,880 559

77.1 22.9

2,726 750

78.4 21.6

5,202 713

87.9 12.1

2,053 386

84.2 15.8

3,149 327

90.6 9.4

1,460 1,481 1,486 1,488

24.7 25.0 25.1 25.2

730 648 581 480

29.9 26.6 23.8 19.7

730 833 905 1,008

21.0 24.0 26.0 29.0

1,468 1,474 1,483 1,490

24.8 24.9 25.1 25.2

711 658 570 500

29.1 27.0 23.4 20.5

757 816 913 990

21.7 23.5 26.3 28.5

4,080 602 653 580

69.0 10.2 11.0 9.8

1,648 248 292 251

67.6 10.2 12.0 10.3

2,432 354 361 329

70.0 10.2 10.4 9.5

5,155 156 604

87.2 2.6 10.2

2,070 74 295

84.9 3.0 12.1

3,085 82 309

88.8 2.4 8.9

1,783 3,235 897

30.1 54.7 15.2

779 1,257 403

31.9 51.5 16.5

1,004 1,978 494

28.9 56.9 14.2

4,298 684 286 647

72.7 11.6 4.8 10.9

1,691 308 146 294

69.3 12.6 6.0 12.1

2,607 376 140 353

75.0 10.8 4.0 10.2

1,445 2,971 1,499

24.4 50.2 25.3

604 1,136 699

24.8 46.6 28.7

841 1,835 800

24.2 52.8 23.0

2,447 3,468

41.4 58.6

688 1,751

28.2 71.8

1,759 1,717

50.6 49.4

4,054 1,380 56 425

68.5 23.3 0.9 7.2

1,678 532 28 201

68.8 21.8 1.1 8.2

2,376 848 28 224

68.4 24.4 0.8 6.4

.3

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⬍ .001

⬍ .001

.1

⬍ .001

⬍ .001

⬍ .001

⬍ .001

⬍ .001

.01

(continued on following page)

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1421

Gandaglia et al

Table 1. Demographics and Clinical Characteristics of Patients Treated for Nonmetastatic Prostate Cancer Between October 2008 and December 2009 Within the SEER-Medicare Database Stratified According to the Surgical Approach (ORP v RARP) (continued) Total

Demographic or Clinical Characteristic

No. of Patients

ORP %

No. of Patients

RARP %

No. of Patients

%

P ⬍ .001

Nodal stage pN0/X pN1 Region Pacific Coast East Northern Plains Southwest

5,786 129

97.8 2.2

2,357 82

96.6 3.4

3,429 47

98.6 1.4

2,048 605 2,865 397

34.6 10.2 48.4 6.7

804 221 1,134 280

33.0 9.1 46.5 11.5

1,244 384 1,731 117

35.8 11.0 49.8 3.4

⬍ .001

Abbreviations: CCI, Charlson comorbidity index; IQR, interquartile range; ORP, open radical prostatectomy; PSA, prostate-specific antigen; PLND, pelvic lymph node dissection; RARP, robotic-assisted radical prostatectomy.

small numbers of PCa diagnoses, each HSA with less than 50 PCa diagnoses was grouped with the neighboring (in terms of the nearest distance with respect to geographic location) HSA that had ⱖ 50 PCa diagnoses.18 Before its use, we assessed the validity of the instrument by confirming that intensity of RARP utilization according to HSA was correlated with receipt of RARP (F statistic ⱖ 10) but was not associated with the outcomes in multivariable models (except for pLOS and postoperative transfusions). Comparative effectiveness of ORP versus RARP was tested through the conventional logistic regression analyses. All statistical testing was two-sided with a level of significance set at P ⫽ .05. Analyses were performed using the R software environment for statistical computing and graphics (version 3.0.1; http://www.r-project.org/).

RESULTS

Use of Robotic Surgery In the SEER-Medicare cohort, 5,915 patients age 65 years or older who underwent RP were identified. Of those, 2,439 patients (41.2%) and 3,476 patients (58.8%) underwent ORP and RARP, respectively. Examination of the overall NIS population demonstrated an increase in the proportion of patients undergoing RARP from 47.8% to 59.7% between October 2008 and December 2009 (Fig 1A; EMPC, 1.70%; P ⫽ .001). Similarly, when focusing on Medicare-eligible men, the rate of RARP use increased from 46.6% to 57.8% (Fig 1B; EMPC, 1.58%; P ⫽ .004). Baseline Characteristics All subsequent analyses relied exclusively on the SEER-Medicare cohort. Average age at diagnosis was 69.1 years (median age, 68 years). When patients were stratified according to surgical approach, statistically significant differences were recorded with respect to age, population density, income, education, clinical stage, Gleason score, prostate-specific antigen, risk group, PLND status, pathologic stage, nodal stage, and region (Table 1; all P ⱕ .01). Bivariate Analyses When focusing on 30-day outcomes, no significant differences were observed in overall complications (Table 2; P ⫽ 0.1). However, patients undergoing RARP had higher rates of genitourinary complications (P ⫽ .001) and lower rates of miscellaneous surgical complications (P ⫽ .01). 1422

© 2014 by American Society of Clinical Oncology

When focusing on 90-day outcomes, patients undergoing RARP had lower rates of overall, respiratory, wound, and miscellaneous medical and surgical complications compared with patients undergoing ORP (Table 2; all P ⱕ .04). Conversely, patients undergoing RARP had higher rates of short-term genitourinary complications (P ⫽ .01). In particular, the most common 30- and 90-day genitourinary complications were urinary complications, not otherwise specified (41.8% and 41.0% of 30- and 90-day genitourinary complications, respectively, in the overall population). Additionally, RARP was associated with lower rates of postoperative transfusions and shorter length of hospital stay (all P ⬍ .001). No differences were observed in 30- and 90-day readmission rates (all P ⱖ .5). The proportion of men receiving adjuvant cancer therapy was lower among patients who underwent RARP compared with ORP (3.6% v 6.3%, respectively; P ⬍ .001). This was confirmed when evaluating the rates of administration of additional treatments anytime after surgery (9.0% for PARP v 12.9% for ORP; P ⬍ .001). Finally, median total first-year charges were more than $1,400 greater for RARP compared with ORP ($13,394.90 v $11,970.40, respectively; P ⬍ .001). Adjusted Perioperative Outcomes Logistic regression analyses revealed comparable overall 30- and 90-day perioperative complications between RARP and ORP (Table 3; P ⱖ .1). However, patients undergoing RARP had higher odds of experiencing genitourinary and miscellaneous medical complications at 30- and 90-day follow-up (all P ⱕ .02). Conversely, RARP patients were less likely to receive a blood transfusion (odds ratio [OR], 0.25; 95% CI, 0.15 to 0.43; P ⬍ .001) and to experience a pLOS (OR, 0.30; 95% CI, 0.24 to 0.37; P ⬍ .001) compared with ORP patients. Surgical approach was not associated with increased odds of use of adjuvant treatments or additional therapies anytime after surgery (all P ⱖ .2). Finally, RARP was significantly associated with higher charges within 1 year from surgery (OR, 1.52; 95% CI, 1.28 to 1.81; P ⬍ .001). DISCUSSION

Despite limited evaluation of the comparative effectiveness between RARP and ORP, as well as the absence of randomized trials comparing JOURNAL OF CLINICAL ONCOLOGY

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Effectiveness of Robot-Assisted Radical Prostatectomy

Table 2. Postoperative Complications, Blood Transfusions, Length of Stay, Additional Cancer Therapy, and Costs Stratified by Surgical Technique for Patients With Prostate Cancer Undergoing Radical Prostatectomy Within the SEER-Medicare Database Between October 2008 and December 2009 Total Factor

No. of Patients

Total patients 30-day postoperative complications Overall Cardiac Respiratory Genitourinary Wound Vascular Miscellaneous medical Miscellaneous surgical 90-day postoperative complications Overall Cardiac Respiratory Genitourinary Wound Vascular Miscellaneous medical Miscellaneous surgical Heterologous blood transfusions Length of stay, daysⴱ Median IQR 30-day readmission rate 90-day readmission rate Additional cancer therapy within 6 months after surgery Overall Radiotherapy Androgen-deprivation therapy Additional cancer therapy anytime after surgery Overall Radiotherapy Androgen-deprivation therapy Median Medicare costs within 12 months from surgery, US dollarsⴱ

5,915

ORP % 100

RARP

No. of Patients

%

No. of Patients

%

2,439

41.2

3,476

58.8

P

1,351 104 297 247 105 127 669 302

22.8 1.8 5.0 4.2 1.8 2.1 11.3 5.1

581 43 134 77 53 54 293 146

23.8 1.8 5.5 3.2 2.2 2.2 12.0 6.0

770 61 163 170 52 73 376 156

22.2 1.8 4.7 4.9 1.5 2.1 10.8 4.5

.1 .9 .1 .001 .05 .8 .2 .01

1,609 119 354 291 127 218 820 362 282

27.2 2.0 6.0 4.9 2.1 3.7 13.9 6.1 4.8

704 49 164 98 66 96 368 176 216

28.9 2.0 6.7 4.0 2.7 3.9 15.1 7.2 8.9

905 70 190 193 61 122 452 186 66

26.0 2.0 5.5 5.6 1.8 3.5 13.0 5.4 1.9

.01 .9 .04 .01 .01 .4 .02 .003 ⬍ .001

2 1-2 230 334 279 210 110 626 494 330 $12,834.9

3.9 5.6

2 2-3 93 143

4.7 3.6 1.9

154 113 61

10.6 8.4 5.6

314 244 164 $11,970.4

⬍ .001

3.8 5.9

1 1-2 137 191

3.9 5.5

.8 .5

6.3 4.6 2.5

125 97 49

3.6 2.8 1.4

⬍ .001 ⬍ .001 .002

312 250 166 $13,394.6

9.0 7.2 4.8

⬍ .001 ⬍ .001 .002 ⬍ .001

12.9 10.0 6.7

Abbreviations: IQR, interquartile range; ORP, open radical prostatectomy; RARP, robotic-assisted radical prostatectomy. ⴱ Based on the Mann-Whitney U test.

the two techniques, RARP was rapidly adopted to become the main surgical approach for treatment of localized PCa. The widespread dissemination of RARP has been largely attributed to market-driven incentives and reproached as a significant contributor to increasing national health care costs related to the treatment of PCa.5,7 As such, the landmark study by Hu et al4 showing no difference between minimally invasive RP and ORP with regard to postoperative complications and long-term functional outcomes was of national interest. Nonetheless, the rapid spread of this new technology and the implicit learning-curve phenomenon associated with this adoption limit the applicability of their findings to patients treated in more contemporary years. Given these considerations, the aim of the current study was to reassess the safety of RARP in the era subsequent to the rapid diffusion of robotic surgery. Although the use of robotic surgery will continue to increase in coming years, the results of the current study were obtained after the period of rapid diffusion for RARP (from 8% to 67% between 2004 and 2010)2 and thus represent the postdissemination era. Acwww.jco.org

cordingly, we assert that, at this point, observed differences between the two surgical approaches may represent technical advantages of one over the other, rather than an effect of the early adoption, although we cannot completely rule out specific providers who started adopting RARP in 2008. Several of our findings are noteworthy. First, our results show that the adoption of RARP has increased significantly between the Hu et al4 study period (2003 to 2007) and the current study period. Specifically, although the use of minimally invasive RP barely attained 45% in the previous study,4 use of RARP relative to ORP was 64% in the last month of the current study period. This trend of RARP utilization was confirmed in the NIS population, where only a slight increase in the utilization rates of robotic surgery was observed over the study period. Second, patients treated with RARP and ORP had similar risk of 30- and 90-day overall postoperative complications and readmission rates, after accounting for measured and unmeasured confounders. However, RARP patients had higher risks of 30- and © 2014 by American Society of Clinical Oncology

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Gandaglia et al

Table 3. Logistic Regression Analysis for Postoperative Complications, Blood Transfusions, Length of Stay, Additional Cancer Therapy, and More Expensive Therapy Stratified by Surgical Technique for Patients With Prostate Cancer Undergoing Radical Prostatectomy Within the SEER-Medicare Database Between October 2008 and December 2009 RARP v ORP Factor 30-day postoperative complications Overall Cardiac Respiratory Genitourinary Wound Vascular Miscellaneous medical Miscellaneous surgical 90-day postoperative complications Overall Cardiac Respiratory Genitourinary Wound Vascular Miscellaneous medical Miscellaneous surgical Heterologous blood transfusions Length of stay ⬎ 2 days 30-day readmission 90-day readmission Additional cancer therapy within 6 months from surgery Overall Radiotherapy Androgen-deprivation therapy Additional cancer therapy anytime after surgery Overall Radiotherapy Androgen-deprivation therapy More expensive therapy within 1 year from surgery

Odds Ratio

95% CI

P

1.19 1.07 0.83 1.93 1.01 0.85 1.45 0.88

0.97 to 1.46 0.56 to 2.02 0.55 to 1.24 1.26 to 2.97 0.55 to 1.85 0.47 to 1.55 1.11 to 1.89 0.61 to 1.30

.1 .8 .3 .002 .9 .6 .01 .5

1.13 1.13 0.88 1.69 0.88 0.86 1.32 0.83 0.25 0.30 1.33 1.08

0.94 to 1.37 0.61 to 2.11 0.61 to 1.28 1.13 to 2.53 0.51 to 1.54 0.54 to 1.36 1.03 to 1.68 0.59 to 1.18 0.15 to 0.43 0.24 to 0.37 0.86 to 2.06 0.75 to 1.56

.2 .7 .5 .01 .6 .5 .02 .3 ⬍ .001 ⬍ .001 .2 .6

0.76 0.83 0.89

0.50 to 1.49 0.52 to 1.32 0.46 to 1.73

.2 .4 .7

0.82 0.89 0.95

0.61 to 1.09 0.65 to 1.23 0.65 to 1.40

.2 .5 .8

1.52

1.28 to 1.81

⬍ .001

NOTE. Model adjusted for age, race, marital status, population density, income, education, baseline Charlson comorbidity index, pelvic lymph node dissection status, Gleason score, clinical stage, and preoperative prostatespecific antigen. Abbreviations: ORP, open radical prostatectomy; RARP, robotic-assisted radical prostatectomy.

90-day genitourinary and miscellaneous medical complications. Although previous studies showed an advantage for RARP compared with ORP in terms of perioperative outcomes,3,19,20 our observations demonstrate that the minimally invasive approach does not represent a safer procedure compared with ORP in Medicare beneficiaries, thus corroborating the findings of Hu et al.4 One possible explanation for these observations may reside in the characteristics of the populations evaluated. Age at surgery and Medicare insurance status represent independent predictors of complications.21,22 Because our analyses and the aforementioned study by Hu et al4 focused exclusively on a population of Medicare beneficiaries age 65 years or older, it is possible that the comparison of the two techniques in different clinical settings would result in significant differences. However, patients undergoing RARP had 1424

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four-fold lower odds of receiving a blood transfusion compared with their ORP counterparts. Additionally, RARP patients had three-fold lower odds of experiencing a pLOS. These findings corroborate previously reported advantages of minimally invasive approaches with regard to blood loss and shorter hospitalization compared with open surgery.3,4,20 Third, we showed that RARP did not increase the risk of receiving additional cancer therapies relative to ORP. These observations have important implications. Historically, the lack of haptic feedback raised concerns regarding the risk of incomplete tumor excision in high-risk patients.23,24 Nonetheless, a meta-analysis performed by Tewari et al19 recently showed that patients undergoing RARP had lower rates of positive surgical margins compared with their open counterparts. These observations, together with the findings of the current study and recently published large institutional series,25 support the safety of RARP. It is conceivable that a more comprehensive visualization of the surgical field, as well as technical advantages related to lower intraoperative bleeding, may lead to equivalent results with regard to additional cancer treatments in these patients. Finally, we assessed expenditures related to surgery using Medicare payment as an approximation of costs.5,26 Interestingly, our results showed that RARP is associated with higher total expenditures within 12 months after surgery compared with ORP. Additionally, patients undergoing RARP had increased odds of receiving more costly therapies within the first year after surgery, even after accounting for confounders. These results are in line with what was previously reported by Lowrance et al26 when analyzing patients undergoing RP included in the SEER-Medicare population. In particular, the authors showed that although patients receiving minimally invasive RP had greater expenditures directly related to surgery, those undergoing ORP had higher expenditures related to additional cancer treatments within the first year after surgery. In this context, the lack of substantial differences with regard to perioperative outcomes and use of additional treatments between the two surgical approaches confirm that higher expenditures for robotic surgery may be directly related to the procedure itself. This has been established in other clinical settings27-29; for example, Kim et al27 recently reported the hospitalization charges for RP in a large population-based cohort from the United States and showed that RARP was approximately $2,500 more costly than ORP. Importantly, our observations emphasize that in the elderly Medicare population, despite these higher hospitalization charges, the adoption of minimally invasive surgery is not counterbalanced by substantial advantages in perioperative outcomes or decreased use of additional treatments. Despite its strengths, our study is not devoid of limitations. First, although the current study sought to emulate a randomized design through advanced statistical methodology, it cannot be considered equivalent to random assignment. Nonetheless, the statistical methodology applied here allows for a robust comparative effectiveness assessment of the two techniques. Indeed, the instrumental variable analysis offers the considerable advantage of minimizing selection bias, thus limiting the effects of unmeasured confounders. Second, although our analyses were performed in the period where RARP has supplanted ORP, surgeon experience still has an important impact on postoperative outcomes.30 To account for this confounder, we relied on an instrumental variable based on the number of robotic procedures performed in a determined geographical area. Third, the nature of our database and the short follow-up of our contemporary cohort JOURNAL OF CLINICAL ONCOLOGY

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Effectiveness of Robot-Assisted Radical Prostatectomy

prevented comparison of oncologic outcomes between the two surgical approaches. Although the use of additional cancer therapies could be considered a proxy for cancer control, given the lack of standardized protocols for the administration of postoperative androgendeprivation therapy and radiotherapy, treating physician preferences likely have introduced an element of heterogeneity when evaluating this outcome. Furthermore, differences between the two surgical approaches with regard to the concomitant receipt of PLND affected nodal staging and thus likely impacted on the subsequent use of additional treatments.31 Moreover, we cannot exclude that the differences in patient characteristics between the two surgical approaches, where a higher proportion of high-risk patients received ORP, may have affected the receipt of postoperative treatments. To address this limitation, our analyses were adjusted for baseline tumor characteristics. Additionally, our study omitted examination of important end points such as postoperative urinary incontinence and erectile dysfunction. Recently, institutional series demonstrated that the adoption of RARP might lead to higher urinary continence recovery rates.32 However, previous population-based studies compared the functional outcomes between the two approaches using a rigorous survey instrument and reported nondifference between the two approaches.33 The short follow-up of patients included in our study prevented comprehensively addressing this issue. Finally, although the professional fees billed by surgeons do vary by surgical approach for patients included in the Medicare program, hospital reimbursement formulas do not vary.5,26 This leads to lower reimbursement for robotic patients included in the Medicare program.27,34 Consequently, we cannot exclude that the difference in expenditures between RARP and ORP may be higher in other clinical settings. RARP and ORP have comparable rates of overall complications and use of additional cancer treatments in our contemporary cohort of patients older than age 65 years treated in a community setting in the period after the broad diffusion of robotic surgery. Conversely, RARP patients had higher risk of genitourinary and miscellaneous medical complications. Consequently, in this population, RARP canREFERENCES 1. Heidenreich A, Bellmunt J, Bolla M, et al: EAU guidelines on prostate cancer: Part 1—Screening, diagnosis, and treatment of clinically localised disease. Eur Urol 59:61-71, 2011 2. Lowrance WT, Eastham JA, Savage C, et al: Contemporary open and robotic radical prostatectomy practice patterns among urologists in the United States. J Urol 187:2087-2092, 2012 3. Novara G, Ficarra V, Rosen RC, et al: Systematic review and meta-analysis of perioperative outcomes and complications after robot-assisted radical prostatectomy. Eur Urol 62:431-452, 2012 4. Hu JC, Gu X, Lipsitz SR, et al: Comparative effectiveness of minimally invasive vs open radical prostatectomy. JAMA 302:1557-1564, 2009 5. Nguyen PL, Gu X, Lipsitz SR, et al: Cost implications of the rapid adoption of newer technologies for treating prostate cancer. J Clin Oncol 29:1517-1524, 2011 6. Close A, Robertson C, Rushton S, et al: Comparative cost-effectiveness of robot-assisted and standard laparoscopic prostatectomy as alternatives to open radical prostatectomy for treatment of men www.jco.org

not be considered a safer approach relative to ORP. Although the benefits associated with the adoption of the minimally invasive approach are represented by lower risk of blood transfusion and by a slight reduction in length of hospital stay, these advantages do not translate into decreased charges relative to open surgery. AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST Although all authors completed the disclosure declaration, the following author(s) and/or an author’s immediate family member(s) indicated a financial or other interest that is relevant to the subject matter under consideration in this article. Certain relationships marked with a “U” are those for which no compensation was received; those relationships marked with a “C” were compensated. For a detailed description of the disclosure categories, or for more information about ASCO’s conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors. Employment or Leadership Position: None Consultant or Advisory Role: None Stock Ownership: None Honoraria: Quoc-Dien Trinh, Intuitive Surgical Research Funding: None Expert Testimony: None Patents, Royalties, and Licenses: None Other Remuneration: None

AUTHOR CONTRIBUTIONS Conception and design: Giorgio Gandaglia, Jesse D. Sammon, Toni K. Choueiri, Pierre I. Karakiewicz, Adam S. Kibel, Francesco Montorsi, Paul L. Nguyen, Mani Menon, Quoc-Dien Trinh Financial support: Pierre I. Karakiewicz, Quoc-Dien Trinh Administrative support: Pierre I. Karakiewicz, Mani Menon, Quoc-Dien Trinh Collection and assembly of data: Giorgio Gandaglia, Jesse D. Sammon, Jim C. Hu, Pierre I. Karakiewicz, Simon P. Kim, Shyam Sukumar, Maxine Sun, Quoc-Dien Trinh Data analysis and interpretation: Giorgio Gandaglia, Jesse D. Sammon, Steven L. Chang, Pierre I. Karakiewicz, Simon P. Kim, Ramdev Konijeti, Quoc-Dien Trinh Manuscript writing: All authors Final approval of manuscript: All authors

with localised prostate cancer: A health technology assessment from the perspective of the UK National Health Service. Eur Urol 64:361-369, 2013 7. Jacobs BL, Zhang Y, Schroeck FR, et al: Use of advanced treatment technologies among men at low risk of dying from prostate cancer. JAMA 309: 2587-2595, 2013 8. Sukumar S, Roghmann F, Trinh VQ, et al: National trends in hospital-acquired preventable adverse events after major cancer surgery in the USA. BMJ Open 3:6, 2013 9. Schmitges J, Trinh QD, Abdollah F, et al: A population-based analysis of temporal perioperative complication rates after minimally invasive radical prostatectomy. Eur Urol 60:564-571, 2011 10. Warren JL, Klabunde CN, Schrag D, et al: Overview of the SEER-Medicare data: Content, research applications, and generalizability to the United States elderly population. Med Care 40:IV-318, 2002 (suppl 8) 11. Klabunde CN, Potosky AL, Legler JM, et al: Development of a comorbidity index using physician claims data. J Clin Epidemiol 53:1258-1267, 2000 12. D’Amico AV, Whittington R, Malkowicz SB, et al: Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial

radiation therapy for clinically localized prostate cancer. JAMA 280:969-974, 1998 13. Jacobs BL, Zhang Y, Tan HJ, et al: Hospitalization trends after prostate and bladder surgery: Implications of potential payment reforms. J Urol 189:59-65, 2013 14. Sheets NC, Hendrix LH, Allen IM, et al: Trends in the use of postprostatectomy therapies for patients with prostate cancer: A Surveillance, Epidemiology, and End Results Medicare analysis. Cancer 119:3295-3301, 2013 15. Williams SB, Amarasekera CA, Gu X, et al: Influence of surgeon and hospital volume on radical prostatectomy costs. J Urol 188:2198-2202, 2012 16. Newhouse JP, McClellan M: Econometrics in outcomes research: The use of instrumental variables. Annu Rev Public Health 19:17-34, 1998 17. Makuc DM, Haglund B, Ingram DD, et al: Health service areas for the United States. Vital Health Stat 2 112:1-102, 1991 18. Lu-Yao G, Albertsen P, Shih W, et al: Failure to report financial disclosure information. JAMA 301: 35-36, 2009 19. Tewari A, Sooriakumaran P, Bloch DA, et al: Positive surgical margin and perioperative complication rates of primary surgical treatments for prostate

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cancer: A systematic review and meta-analysis comparing retropubic, laparoscopic, and robotic prostatectomy. Eur Urol 62:1-15, 2012 20. Trinh QD, Sammon J, Sun M, et al: Perioperative outcomes of robot-assisted radical prostatectomy compared with open radical prostatectomy: Results from the nationwide inpatient sample. Eur Urol 61:679-685, 2012 21. Liu JJ, Maxwell BG, Panousis P, et al: Perioperative outcomes for laparoscopic and robotic compared with open prostatectomy using the National Surgical Quality Improvement Program (NSQIP) database. Urology 82:579-583, 2013 22. Trinh QD, Schmitges J, Sun M, et al: Morbidity and mortality of radical prostatectomy differs by insurance status. Cancer 118:1803-1810, 2012 23. Williams SB, Chen MH, D’Amico AV, et al: Radical retropubic prostatectomy and roboticassisted laparoscopic prostatectomy: Likelihood of positive surgical margin(s). Urology 76:1097-1101, 2010

24. Lee EK, Baack J, Duchene DA: Survey of practicing urologists: Robotic versus open radical prostatectomy. Can J Urol 17:5094-5098, 2010 25. Menon M, Bhandari M, Gupta N, et al: Biochemical recurrence following robot-assisted radical prostatectomy: Analysis of 1384 patients with a median 5-year follow-up. Eur Urol 58:838-846, 2010 26. Lowrance WT, Eastham JA, Yee DS, et al: Costs of medical care after open or minimally invasive prostate cancer surgery: A population-based analysis. Cancer 118:3079-3086, 2012 27. Kim SP, Shah ND, Karnes RJ, et al: Hospitalization costs for radical prostatectomy attributable to robotic surgery. Eur Urol 64:11-16, 2013 28. Yu HY, Hevelone ND, Lipsitz SR, et al: Hospital volume, utilization, costs and outcomes of robotassisted laparoscopic radical prostatectomy. J Urol 187:1632-1637, 2012 29. Yu HY, Hevelone ND, Lipsitz SR, et al: Use, costs and comparative effectiveness of robotic assisted, laparoscopic and open urological surgery. J Urol 187:1392-1398, 2012

30. Sammon JD, Karakiewicz PI, Sun M, et al: Robot-assisted versus open radical prostatectomy: The differential effect of regionalization, procedure volume and operative approach. J Urol 189:12891294, 2013 31. Feifer AH, Elkin EB, Lowrance WT, et al: Temporal trends and predictors of pelvic lymph node dissection in open or minimally invasive radical prostatectomy. Cancer 117:3933-3942, 2011 32. Montorsi F, Wilson TG, Rosen RC, et al: Best practices in robot-assisted radical prostatectomy: Recommendations of the Pasadena Consensus Panel. Eur Urol 62:368-381, 2012 33. Barry MJ, Gallagher PM, Skinner JS, et al: Adverse effects of robotic-assisted laparoscopic versus open retropubic radical prostatectomy among a nationwide random sample of Medicare-age men. J Clin Oncol 30:513-518, 2012 34. Lotan Y, Bolenz C, Gupta A, et al: The effect of the approach to radical prostatectomy on the profitability of hospitals and surgeons. BJU Int 105:15311535, 2010

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GLOSSARY TERMS

Gleason score: a pathologic description of prostate cancer grade on the basis of the degree of abnormality in the glandular architecture. Gleason patterns 3, 4, and 5 denote low, intermediate, and high levels of histologic abnormality and tumor aggressiveness, respectively. The score assigns primary and secondary numbers on the basis of the most common and second most common patterns identified.

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© 2014 by American Society of Clinical Oncology

prostate-specific antigen (PSA): a protein produced by cells of the prostate gland. The blood level of PSA is used as a tumor marker for men who may be suspected of having prostate cancer. Most physicians consider 0 to 4.0 ng/mL as the normal range. Levels of 4 to 10 and 10 to 20 ng/mL are considered slightly and moderately elevated, respectively. PSA levels have to be complemented with other tests to make a firm diagnosis of prostate cancer.

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Appendix

Table A1. Diagnostic and Procedures Codes Used to Identify 30- and 90-Day Postoperative Complications and the Use of Additional Cancer Therapy After Surgery Category Cardiac

Respiratory

Genitourinary

Diagnosis Codes (ICD-9) 410.xx (acute myocardial infarction), 402.01, 402.11, 402.91, 428.xx (heart failure), 427.5 (cardiac arrest), 997.1 (cardiac complications, NOS) 518.0 (pulmonary collapse), 514 (pulmonary congestion and hypostasis), 518.4 (acute edema of lung, unspecified), 466.xx (acute bronchitis and bronchiolitis), 480.xx (viral pneumonia), 481 (pneumococcal pneumonia), 482.xx (other bacterial pneumonia), 483.xx (pneumonia due to other specified organisms), 485 (bronchopneumonia, organism unspecified), 486 (pneumonia, organism unspecified), 518.5 (pulmonary insufficiency following surgery), 518.81 (acute respiratory failure), 518.82 (other pulmonary insufficiency, NOS), 799.1 (respiratory arrest), 997.3 (respiratory complications, NOS) 590.1x (acute pyelonephritis), 590.2 (renal and perinephric abscess), 590.8x (other pyelonephritis or pyonephrosis, NOS), 590.9 (infection of the kidney), 591 (hydronephrosis), 593.3 (stricture of ureter), 593.4 (other ureteric obstruction), 593.5 (hydroureter), 593.81 (vascular disorders of the kidney), 593.82 (ureteral fistula), 595.89 (abscess of the bladder, cystitis), 596.1 (intestinovesical fistula), 596.2 (vesical fistula, NOS), 596.6 (rupture of bladder), 997.5 (urinary complications, NOS), 599.1 (urethral fistula)

Wound

567.xx (peritonitis and retroperitoneal infections), 998.3 (disruption of wound), 998.5x (infected postoperative seroma and other postoperative infection), 998.6 (postoperative fistula)

Vascular

451.1x, 451.2, 451.81, 451.9 (phlebitis and thrombophlebitis), 453.8, 453.9 (venous embolism and thrombosis), 997.2 (peripheral vascular complications), 999.2 (other vascular complications, NOS), 444.22, 444.81 (arterial embolism and thrombosis), 433.xx (occlusion and stenosis of precerebral arteries), 434.xx (occlusion of cerebral arteries), 436 (acute cerebrovascular disease), 437.xx (other cerebrovascular disease, NOS)

Procedure Codes (ICD-9, CPT, and HCPCS)

ICD-9: 55.02 (nephrostomy), 55.03 (percutaneous nephrostomy with fragmentation), 55.12 (pyelostomy), 55.93 (replacement of nephrostomy tube), 55.94 (replacement of pyelostomy tube), 97.61 (removal of pyelostomy and nephrostomy tube), 97.62 (removal of ureterostomy tube), 56.1 (ureteral meatotomy), 56.41 (partial ureterectomy), 56.74 (ureteroneocystostomy), 56.75 (transureteroureterostomy), 56.81 (lysis of intraluminal adhesion of ureter), 56.84 (closure of other fistula of ureter), 56.86 (removal of ligature from ureter), 56.89 (other repair of the ureter), 56.91 (dilatation of ureteral meatus) CPT: 50040 (nephrostomy), 50120 (pyelostomy), 50125 (pyelostomy with drainage), 50395 (percutaneous nephrostomy), 50398 (change of nephrostomy), 50605 (ureterotomy), 52290, 52332, 52334 (cystourethroscopy including ureteral catheterization), 50600 (ureterotomy with exploration or drainage), 50700 (ureteroplasty), 50715 (ureterolysis), 50760 (ureteroureterostomy), 50770 (transureteroureterostomy), 50780, 50782, 50783, 50785 (ureteroneocystostomy), 50800 (ureteroenterostomy), 50810 (ureterosigmoidostomy), 50815 (ureterocolon conduit), 50820 (ureteroileal conduit), 50825 (continent diversion), 50840 (replace all or part of the ureter by intestine segment), 50900 (ureterorrhaphy), 50940 (deligation of ureter) ICD-9: 54.61 (reclosure of postoperative disruption of abdominal wall), 54.1x (laparotomy), 54.91 (percutaneous abdominal drainage), 54.0 (incision of abdominal wall), 59.19 (incision of hematoma of space of Retzius) CPT: 26990 (incision and drainage of deep abscess or hematoma), 45020 (incision and drainage of deep supralevator, pelvirectal, or retrorectal abscess), 49060 (drainage of retroperitoneal abscess), 51,080 (drainage of perivesical or prevesical space abscess)

(continued on following page)

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Table A1. Diagnostic and Procedures Codes Used to Identify 30- and 90-Day Postoperative Complications and the Use of Additional Cancer Therapy After Surgery (continued) Category

Diagnosis Codes (ICD-9)

Miscellaneous medical

584.xx (acute renal failure), 586 (renal failure, NOS), 785.5x (shock), 995.4 (shock due to anesthesia), 998.7, 998.0 (other complications of procedures), 999.4, 999.5, 999.6, 999.7, 999.8 (complications of medical care), 457.8 (noninfectious disorders of lymphatic channels), 560.1, 560.8x, 560.9 (intestinal obstruction without mention of hernia), 997.4 (digestive system complications, NOS), 353.0 (brachial plexus lesion), 354.2 (lesion of ulnar nerve), 723.4 (brachia neuritis or radiculitis, NOS), 955.1, 955.3, 955.7, 955.8, 955.9 (injury to peripheral nerve of shoulder girdle and upper limb), 593.4 (other ureteric obstruction, idiopathic), 531.xx (gastric ulcer), 532.xx (duodenal ulcer), 533.xx (peptic ulcer), 782.4 (jaundice, unspecified), 573.8 (liver disorders, NOS) 565.1 (anal fistula), 569.3, 569.83, 569.4x (other disorders of the intestine), 998.1x (hemorrhage or hematoma or seroma complicating a procedure), 998.83 (nonhealing surgical wound), 998.9 (unspecified complication of procedure), 998.2 (accidental puncture or laceration during a procedure), 998.4 (foreign body accidentally left during a procedure), 604.0 (orchitis, epididymitis, and epididymo-orchitis, with abscess), E870.0 (surgical operation), E870.4 (endoscopic examination), E870.7 (administration of enema), E870.8, E870.9 (other specified medical care), E871.0 (surgical operation), E873.0 (excessive amount of blood or other fluid during transfusion or infusion), E876.0 (mismatched blood in transfusion), 956.0, 956.1, 956.4, 956.5, 956.8, 956.9 (injury to peripheral nerves of pelvic girdle and lower limb), 902.50, 902.51, 902.52, 902.53, 902.54, 902.59 (injury of blood vessels of abdomen and pelvis) V58.2

Miscellaneous surgical

Blood transfusion

Hormonal therapy

Radiotherapy

Procedure Codes (ICD-9, CPT, and HCPCS)

ICD-9: 46.03 (exteriorization of large intestine), 46.04 (resection of exteriorized segment of large intestine), 46.10 (colostomy, NOS), 46.11 (temporary colostomy), 46.14 (delayed opening of colostomy), 48.4x (pull-through resection of rectum), 48.5 (abdominoperineal resection of rectum), 48.6x (other resection of rectum), 48.7x (repair of rectum), 48.9x (other operations on rectum and perirectal tissue)

ICD-9: 99.04 CPT: 86930, 86965, 86999 HCPCS: P9010, P9011, P9017, P9021, P9022, P9038, P9039, P9040 ICD-9: 62.41 CPT: 54520 HCPCS: C9216, C9430, G0356, J0128, J3315, J9202, J9217, J9218, J9219, S0165, S9560 ICD-9: 92.2x CPT: 76965, 77301, 77305, 77310, 77315, 77331, 77371, 77372, 77373, 77399, 77401, 77402, 77403, 77404, 77406, 77407, 77408, 77409, 77411, 77412, 77413, 77414, 77416, 77418, 77421, 77422, 77423, 77427, 77431, 77440, 77499, 77520, 77522, 77523, 77525, 79300, 79440, 79999, 4201F, 4210F, 4165F, 79200 HCPCS: G0174, G0242, G0243

Abbreviations: CPT, current procedural terminology; HCPCS, Healthcare Common Procedure Coding System; ICD-9, International Classification of Diseases, Ninth Edition; NOS, not otherwise specified.

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