Risk of Small Bowel Obstruction After Robot-Assisted vs Open Radical Prostatectomy

Abstract

Background and Purpose:

Whereas open radical prostatectomy is performed extraperitoneally, minimally invasive radical prostatectomy is typically performed within the peritoneal cavity. Our objective was to determine whether minimally invasive radical prostatectomy is associated with an increased risk of small bowel obstruction compared with open radical prostatectomy.

Patients and Methods:

In the U.S. Surveillance, Epidemiology and End Results (SEER)-Medicare database, we identified 14,147 men found to have prostate cancer from 2000 to 2008 treated by open (n = 10,954) or minimally invasive (n = 3193) radical prostatectomy. Multivariable Cox proportional hazard models were used to examine the impact of surgical approach on the diagnosis of small bowel obstruction, as well as the need for lysis of adhesions and exploratory laparotomy.

Results:

During a median follow-up of 45 and 76 months, respectively, the cumulative incidence of small bowel obstruction was 3.7% for minimally invasive and 5.3% for open radical prostatectomy (p = 0.0005). Lysis of adhesions occurred in 1.1% of minimally invasive and 2.0% of open prostatectomy patients (p = 0.0003). On multivariable analysis, there was no significant difference between minimally invasive and open prostatectomy with respect to small bowel obstruction (HR 1.17, 95% CI 0.90, 1.52, p = 0.25) or lysis of adhesions (HR 0.87, 95% CI 0.50, 1.40, p = 0.57). Limitations of the study include the retrospective design and use of administrative claims data.

Conclusions:

Relative to open radical prostatectomy, minimally invasive radical prostatectomy is not associated with an increased risk of postoperative small bowel obstruction and lysis of adhesions.

Introduction

Over the past decade, there has been a dramatic shift in the approach to the surgical management of prostate cancer. This includes fewer open radical retropubic prostatectomy (RRP) and increasing use of minimally invasive radical prostatectomy (MIRP), which is primarily performed robotically.

Robot-assisted radical prostatectomy (RARP) remains expensive, including the upfront purchasing costs for the robotic platform, as well as annual mandatory service fees and disposable instruments used for each case.¹ Despite a shorter length of stay with robotic prostatectomy in some studies,² other studies have shown a similar length of stay and care pathway irrespective of surgical approach³ or even a greater number of robotic patients falling “off pathway” because of ileus.⁴ Furthermore, a recent study by Gandaglia and colleagues reported that at 1 year the cost of robotic prostatectomy remains significantly higher than open prostatectomy.⁵

Although patients perceive that robotic prostatectomy will reduce complications,⁶ large studies using validated questionnaires have reported no clinically significant differences in health-related quality of life (Patient Oriented Prostate Utility Scale-Psychometric [PORPUS-P]), erectile function (International Index of Erectile Dysfunction [IIEF]), or urinary symptoms (International Prostate Symptom Score [IPSS]).⁷ For example, a randomized trial of robotic vs open radical prostatectomy (ORP) in Australia found no difference in sexual or urinary function at 12 weeks.² Another recent study reported no significant difference in overall complications between RRP and MIRP,⁵ although the frequency of specific types of complications varied based on surgical approach. MIRP had a significantly higher frequency of genitourinary and miscellaneous medical complications during the first 3 months, while RRP had a significantly higher risk of blood transfusions and prolonged hospitalization.

With regard to abdominal complications, one previous study reported a significantly higher risk of hernia among men treated by MIRP.⁸ Less is known about the comparative risk of small bowel obstruction (SBO) between MIRP and ORP. A recent study from Sweden found a significantly higher frequency of admission for SBO during the first year after MIRP compared with ORP, but no difference at 5 years.⁹

SBO is potentially a major complication, which is often ensued by a lysis of adhesions (LOA). Since MIRP is typically performed through the abdomen (transperitoneal) and RRP is done through the pelvis (extraperitoneal), our hypothesis was that MIRP would therefore result in more adhesion formation, increasing the risk of SBO and LOA.

Patients and Methods

Data source

Data originated from the National Cancer Institute's Surveillance, Epidemiology and End Results (SEER) program of cancer registries that collect clinical, demographic, and cause of death information for persons with cancer in the United States. SEER data were linked to claims data provided by the Center for Medicare and Medicaid Services (CMS) for covered healthcare services from the time of Medicare eligibility until death. For the linkage, 93% of men aged 65 years and older in the SEER files were matched to the Medicare enrolment file.¹⁰

Study population

We identified 16,107 patients with histologically confirmed prostate cancer (PCa) (International Classification of Disease for Oncology [ICD-O] site code 61.9, histologic code 8140), aged ≥66 years, diagnosed and treated with RP within 1 year of diagnosis, between January 1, 2000 and December 31, 2008.

Patients who underwent MIRP were identified by searching for concomitant robot-assisted (ICD-9 Clinical Modification [ICD-9-CM] procedure code: 17.42) or laparoscopic modifiers (CPT code: 55866). Patients who underwent ORP were identified using CPT codes: 55840, 55842, and 55845. Exclusion criteria consisted of metastatic disease (n = 315), pathologic stage other than T2 or T3, clinical tumor stage T4 (n = 1115), unknown/anaplastic/undifferentiated tumor grade (n = 105), and history of SBO in the year prior to RP (n = 113). Moreover, patients with the diagnosis of Crohn's Disease or Ulcerative Colitis 1 year before surgery were excluded (n = 312). Following these exclusions, the final study sample included 14,147 men, of which 10,954 underwent ORP and 3193 underwent MIRP.

Covariates and end points

We retrieved the following demographic and clinical data for all participants: age at diagnosis, year of diagnosis, year of surgery, race (white, black, other), and receipt of pelvic lymph node dissection (PLND). In addition, Gleason score and American Joint Committee on Cancer (AJCC) clinical stage were available. Before 2003, Gleason grades of 2 to 4, 5 to 7, and 8 to 10 corresponded to well, moderately, and poorly differentiated disease, respectively, whereas thereafter a Gleason grade of 2 to 4, 5 to 6, and 7 to 10 corresponded to well, moderately, and poorly differentiated PCa, respectively. Well and moderately differentiated cancers constitute the low-risk group. The Charlson comorbidity index (CCI) was derived from the Medicare claims 1 year before PCa diagnosis and categorized as 0, 1, 2+ using a previously validated algorithm.¹¹ Receipt of pelvic radiation therapy was ascertained using procedure codes. The primary outcomes of interest were diagnosis of SBO and LOA after radical prostatectomy (see Appendix 1 for codes).

Statistical analyses

Summary statistics were constructed using frequencies and proportions for categorical variables, as well as medians and interquartile ranges for continuous variables. Categorical values were compared using chi-square test, and continuous variables were compared with the Wilcoxon rank sum test. A Cox proportional hazard model with competing risk of death was constructed to examine the impact of surgical approach (MIRP vs ORP) on the risk of developing SBO, adjusting for age (per 1 year increase), Charlson index (per 1 unit increase), year of surgery (per 1 year increase), race, grade, pathologic stage, lymph node dissection, and receipt of radiotherapy. A separate Cox proportional hazard model was used to examine the impact of surgical approach on LOA.

All statistical testing was two sided with a level of significance set at 0.05. Analyses were performed using SAS, version 9.3 (SAS Institute, Cary, North Carolina). An institutional review board waiver was obtained before conducting this study, in accordance with institutional regulation when dealing with de-identified administrative data.

Results

Table 1 shows the demographics of the study population. The median overall age was 69 years, 87% was white, and most men had Charlson comorbidity scores of 0, with no significant difference in age or comorbidity between the groups. Men undergoing MIRP were less likely to be African American, more likely to live in metropolitan areas, with a significantly higher income and educational level in the census tract, with more PSA-detected cancers but a higher risk group. RRP patients were more likely to undergo PLND, to receive radiation therapy, and to undergo MIRP in more recent years.

Table 1.

Demographic, Clinical, and Pathologic Features of Men Undergoing Minimally Invasive and Open Radical Prostatectomy Without Crohn's or Ulcerative Colitis 1 Year Prior

	Total population N = 14,147	MIRP, N = 3193	RRP, N = 10,954	p
Age at diagnosis
Mean	70.12	70.10	70.13	0.39
Median (IQR)	69.50 (67.67, 72.08)	69.42 (67.59, 72.00)	69.50 (67.67, 72.08)
Year of diagnosis
2000–2004	7780 (54.99)	422 (13.22	7358 (67.17)	<0.0001
2005–2008	6367 (45.01)	2771 (86.78)	3596 (32.83)
Year of surgery
2000–2004	7490 (52.94)	332 (10.40)	7158 (65.35)	<0.0001
2005–2008	6657 (47.06)	2861 (89.60)	3796 (34.65)
Region
Midwest	1668 (11.79)	401 (12.56)	1267 (11.57)	<0.0001
Northeast	1716 (12.13)	522 (16.35)	1194 (10.90)
South	3009 (21.27)	517 (16.19)	2492 (22.75)
West	7754 (54.81)	1753 (54.90)	6001 (54.78)
Population density
Metropolitan	11,894 (84.07)	2849 (89.23)	9045 (82.57)	<0.0001
Nonmetropolitan	2253 (15.93)	344 (10.77)	1909 (17.43)
Race
White	12,347 (87.28)	2785 (87.22)	9562 (87.29)	<0.0001
African American	939 (6.64)	170 (5.32)	769 (7.02)
Other	861 (6.09)	238 (7.45)	623 (5.69)
Marital status
Married	11,602 (82.01)	2628 (82.31)	8974 (81.92)	0.0330
Unmarried	2005 (14.17)	423 (13.25)	1582 (14.44)
Unknown	540 (3.82)	142 (4.45)	398 (3.63)
Annual median income ($)	48920.0 (37100.0, 66882.0)	54635.0 (40413.0, 75098.0)	47348.5 (36401.5, 64890.0)	<0.0001
College education (%)	24.97 (14.28, 42.30)	29.20 (16.65, 47.57)	23.70 (13.77, 40.16)	<0.0001
CCI
0	11,005 (77.79)	2498 (78.23)	8507 (77.66)	0.3493
1	2496 (17.64)	540 (16.91)	1956 (17.86)
2+	646 (4.57)	155 (4.85)	491 (4.48)
Clinical stage
T1	6860 (48.49)	1910 (59.82)	4950 (45.19)	<0.0001
T2	7041 (49.77)	1231 (38.55)	5810 (53.04)
T3	246 (1.74)	52 (1.63)	194 (1.77)
Risk group^a
Low risk	7319 (51.74)	1131 (35.42)	6188 (56.49)	<0.0001
High risk	6828 (48.26)	2062 (64.58)	4766 (43.51)
Pathologic stage
T2	10,302 (72.82)	2482 (77.73)	7820 (71.39)	<0.0001
T3	3845 (27.18)	711 (22.27)	3134 (28.61)
Radiation therapy (%)	2502 (17.69)	414 (12.97)	2088 (19.06)	<0.0001
PLND done (%)	10,416 (73.63)	1473 (46.13)	8943 (81.64)	<0.0001

Before 2003, Gleason grade of 2 to 4, 5 to 7, and 8 to 10 corresponded to well-differentiated (AJCC grade 1), moderately (AJCC grade 2) differentiated, and poorly differentiated disease (AJCC grade 3), respectively. Thereafter, a Gleason grade of 2 to 4, 5 to 6, and 7 to 10 corresponded to well-differentiated, moderately differentiated, and poorly differentiated PCa. Well and moderately differentiated cancers constitute the low risk group.

AJCC, American Joint Committee on Cancer; CCI, Charlson comorbidity index; MIRP = minimally invasive radical prostatectomy; PCa = prostate cancer; PLND = pelvic lymph node dissection; RRP = radical retropubic prostatectomy.

There was a substantial shift over time with the vast majority of RRP performed during the early years of the study and more MIRP during the later years of the study. Correspondingly, the postoperative follow-up time for assessment of SBO and LOA was significantly less for men undergoing MIRP (Table 2). The cumulative incidence of SBO was 3.7% for MIRP and 5.3% for RRP. LOA occurred in 1.1% of MIRP and 2.0% of RRP during the unequal follow-up periods.

Table 2.

Frequency of Small Bowel Obstruction and Lysis of Adhesions After Minimally Invasive vs Open Radical Prostatectomy

	Total population, N = 14,147	Robot/Lap, N = 3193s	Open, N = 10,954	p
SBO	694 (4.91)	119 (3.73)	575 (5.25)	0.0005
Follow-up to SBO (months)
Mean	69.27	45.37	76.23	<0.0001
Median (IQR)	67.04 (42.48, 95.97)	42.58 (32.55, 56.45)	78.11 (50.47, 102.97)
LOA	253 (1.79)	36 (1.13)	217 (1.98)	0.001
Follow-up to LOA (months)
Mean	70.58	46.35	77.64	<0.0001
Median (IQR)	68.48 (43.73, 97.22)	43.04 (33.24, 56.91)	79.53 (52.34, 103.89)

LOA = lysis of adhesions; SBO = small bowel obstruction.

In the adjusted multivariable Cox proportional hazard model (Table 3), MIRP vs open RRP was not significantly associated with SBO (HR 1.17, 95% CI 0.90, 1.52, p = 0.25). Similarly, there was no significant association between the surgical approach with LOA on multivariable analysis (HR 0.87, 95% CI 0.50, 1.40, p = 0.57). Increasing age was a significant predictor of both SBO and LOA, while higher comorbidity scores also predicted a greater risk of SBO. More recent year of surgery was associated with decreased likelihood of SBO and LOA.

Table 3.

Multivariable Cox Proportional Hazard Models with Death as a Competing risk for (a) Small Bowel Obstruction and (b) Lysis of Adhesions After Radical Prostatectomy in Men Without the Diagnosis of Crohn's or Ulcerative Colitis 1 Year Before Their Prostatectomy

(a)
	HR (95% CI)	p
MIRP vs Open	1.17 (0.90, 1.52)	0.25
Charlson index (1 unit increase)	1.13 (0.99, 1.29)	0.07
Age at diagnosis (1 year increase)	1.05 (1.03, 1.08)	<0.0001
Year of surgery (1 year increase)	0.93 (0.89, 0.97)	0.0002
Grade (high vs low risk)	1.23 (1.04, 1.46)	0.02

(b)
	HR (95% CI)	p
MIRP vs Open	0.87 (0.50, 1.40)	0.57
Charlson index (1 unit increase)	0.99 (0.79, 1.23)	0.90
Age at diagnosis (1 year increase)	1.07 (1.03, 1.10)	0.0007
Year of surgery (1 year increase)	0.93 (0.71, 0.99)	0.021
Grade (high vs low risk)	1.40 (1.06, 1.86)	0.02

(Adjustments made for year of surgery, race, Charlson category, grade and pathologic stage, lymph node dissection, and receipt of radiotherapy.)

These results were further confirmed in subset analyses, when stratified according to the use of PLND and when excluding patients with a prior history of radiotherapy or hernia.

Discussion

Advantages to performing minimally invasive prostatectomy using a transperitoneal approach include a wider working space and shorter time required to prepare the field. However, disadvantages of this approach notably include contact with the bowels, which may directly or indirectly (through the use of foreign bodies and products) induce scarring and adhesions.¹² On the basis of these considerations, and given that RRP is extraperitoneal, many have hypothesized that MIRP may be associated with an increased risk of SBO. In a large population of men from the U.S. SEER-Medicare linked dataset, we found no significant association between prostatectomy approach (MIRP vs RRP) with subsequent SBO or LOA.

Several small studies have compared the risk of complications after transperitoneal vs extraperitoneal robotic prostatectomy. For example, Akand and colleagues prospectively randomized 120 men to either of the two approaches for RARP between 2011 and 2014.¹³ Extraperitoneal RARP was associated with significantly greater trocar insertion time, shorter console time, lower blood loss, shorter hospitalization, and shorter time for beginning an oral diet (20.1 hours vs 32.3 hours, p = 0.031). Despite one case of paralytic ileus in the transperitoneal group, there was no significant difference in overall postoperative complications between the two groups. Horstmann and colleagues reported a nonrandomized comparison of 170 patients treated by extraperitoneal vs transperitoneal RARP at their institution.¹⁴ In this study, the extraperitoneal approach had a lower complication rate and significantly shorter time until first defecation (2.6 days vs 3.0 days, p = 0.0131). Bowel-related complications occurred in 1 (1%) extraperitoneal and 3 (4.5%) transperitoneal cases. Finally, Chung and colleagues also performed a nonrandomized comparison of 155 extraperitoneal vs 105 transperitoneal RARP.¹⁵ Unlike the previous studies, there was no difference between techniques in the mean time until normal diet (p = 1.000). However, ileus occurred in 0% extraperitoneal vs 6.7% of the transperitoneal cases.

Concerning other types of abdominal complications, Carlsson and colleagues found that MIRP was significantly associated with an increased risk of incisional hernia.⁸ Another study by Luz and colleagues showed that transperitoneal MIRP increases the amount of small bowel that would receive dosing of salvage radiation,¹⁶ which might potentially impact the risk of subsequent abdominal complications. Conversely, another study by Finelli and colleagues objected this finding by finding a 16% overlap rate between small bowel targeting volume between laparoscopic and open RRP (p = 0.579).¹⁷

One limitation of this study is the use of Medicare data, which excludes men younger than age 65. It is possible that the method of RP and risk of complications may differ between younger and older men, so these results may not be a reflection of the whole population. Moreover, our study relied on administrative claims, for which procedural claims are more likely to be accurate than diagnostic codes for SBO. Third, our study may not account for previous abdominal surgeries performed more than a year before RP. Patients with a complex history of abdominal surgeries may have been preferentially referred to RRP, which may bias our results. Finally, we could not account for other unmeasured confounders such as differences in tissue handling during MIRP.

Conclusions

In conclusion, we found no association between open vs minimally invasive approach to radical prostatectomy and the risk of SBO or LOA.

Footnotes

Acknowledgments

Q.-D.T. is supported by an unrestricted educational grant from the Vattikuti Urology Institute, a Clay Hamlin Young Investigator Award from the Prostate Cancer Foundation, and a Genentech BioOncology Career Development Award from the Conquer Cancer Foundation of the American Society of Clinical Oncology. S.L. is supported by the Laura & Isaac Perlmutter NYU Cancer Center and the Louis Feil Charitable Lead Trust.

Author Disclosure Statement

A.S.K.: Consultant for Sanofi, Astellas, Genzyme, LR Squibbs; Q.-D.T.: Honoraria from Surgical Intuitive; S.L., C.P.M., G.R., C.C., H.L.: No competing financial interests exist.

Abbreviations Used

Appendix 1.

ICD-9 and CPT Codes

Condition	ICD-9 Code	CPT Code
Small bowel obstruction	560.81, 560.89, 560.9
Lysis of adhesions	54.5	44005, 44180
Crohn's disease	555.0, 555.1, 555.2, 555.9
Ulcerative colitis	556.0, 556.1, 556.2, 556.3, 556.4, 556.5, 556.6, 556.8, 556.9

ICD-9 = International Classification of Diseases 9th edition.

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