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| Clinical outcomes for men with positive surgical margins after radical prostatectomy—results from the South Australian Prostate Cancer Clinical Outcomes Collaborative community-based registry |
Kerri R. Beckmanna,b,*( ),Michael E. O'Callaghanc,Andrew D. Vincentd,Kim L. Morettia,c,e,Nicholas R. Brookf
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aCancer Epidemiology and Population Health Research, University of South Australia, Adelaide, Australia
bTranslational Oncology and Urology Research, Division of Pharmaceutical and Cancer Studies, Kings College London, London, UK
cSouth Australian Prostate Cancer Clinical Outcomes Collaborative, Flinders Medical Centre, Adelaide, Australia
dThe Freemason's Foundation Centre for Men's Health, Adelaide Medical School, University of Adelaide, Adelaide, Australia
eDiscipline of Surgery, University of Adelaide, Adelaide, Australia
fDepartment of Urology, Royal Adelaide Hospital, Adelaide, Australia |
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Abstract Objective: Positive surgical margins (PSMs) after radical prostatectomy (RP) indicate failure of surgery to completely clear cancer. PSMs confer an increased risk of biochemical recurrence (BCR), but how more robust outcomes are affected is unclear. This study investigated factors associated with PSMs following RP and determined their impact on clinical outcomes (BCR, second treatment [radiotherapy and/or androgen deprivation therapy], and prostate cancer-specific mortality [PCSM]). Methods: The study cohort included men diagnosed with prostate cancer (pT2-3b/N0/M0) between January 1998 and June 2016 who underwent RP from the South Australian Prostate Cancer Clinical Outcomes Collaborative database. Factors associated with risk of PSMs were identified using Poisson regression. The impact of PSMs on clinical outcomes (BCR, second treatment, and PCSM) was assessed using competing risk regression. Results: Of the 2827 eligible participants, 28% had PSMs—10% apical, 6% bladder neck, 17% posterolateral, and 5% at multiple locations. Median follow-up was 9.6 years with 81 deaths from prostate cancer recorded. Likelihood of PSM increased with higher pathological grade and pathological tumor stage, and greater tumour volume, but decreased with increasing surgeon volume (odds ratio [OR]: 0.93; 95% confidence interval [CI]: 0.88-0.98, per 100 previous prostatectomies). PSMs were associated with increased risk of BCR (adjusted sub-distribution hazard ratio [sHR] 2.5; 95% CI 2.1-3.1) and second treatment (sHR 2.9; 95% CI 2.4-3.5). Risk of BCR was increased similarly for each PSM location, but was higher for multiple margin sites. We found no association between PSMs and PCSM. Conclusion: Our findings support previous research suggesting that PSMs are not independently associated with PCSM despite strong association with BCR. Reducing PSM rates remains an important objective, given the higher likelihood of secondary treatment with associated comorbidities.
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Received: 28 May 2021
Available online: 20 October 2023
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Corresponding Authors:
*Cancer Epidemiology and Population Health Research, University of South Australia, Adelaide, Australia. E-mail address: kerri.beckmann@unisa.edu.au (K.R. Beckmann).
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| Characteristic | Margin status | Margin locationb | Multiplicity | | Negative | Positive | Apical | Bladder neck | Posterolateral | Single site | Multi-sites | | Total, n (%) | 2030 (72) | 797 (28) | 289 (10) | 172 (6) | 470 (17) | 652 (23) | 145 (5) | | NCCN risk category at Dx, n (%)c | | Low | 568 (78) | 159 (22) | 57 (8) | 30 (4) | 85 (8) | 142 (18) | 17 (2) | | Intermediate | 1232 (71) | 493 (29) | 189 (12) | 87 (5) | 314 (19) | 391 (24) | 102 (6) | | High | 230 (61) | 145 (39) | 43 (11) | 55 (15) | 71 (19) | 119 (32) | 26 (7) | | Gleason score at RP, n (%)c | | ≤6 | 502 (80) | 126 (20) | 52 (8) | 19 (3) | 60 (10) | 115 (18) | 11 (2) | | 3+4 | 932 (72) | 356 (28) | 133 (10) | 58 (5) | 215 (17) | 296 (23) | 60 (5) | | 4+3 | 416 (68) | 199 (32) | 61 (10) | 52 (8) | 127 (21) | 157 (26) | 42 (7) | | 8 | 103 (67) | 51 (33) | 19 (12) | 18 (12) | 31 (20) | 35 (23) | 16 (10) | | 9-10 | 70 (52) | 64 (48) | 24 (18) | 24 (18) | 37 (28) | 48 (36) | 16 (12) | | Missing | 7 | 1 | 0 | 0 | 0 | 1 | 0 | | Pathological stage, n (%)c | | pT2 | 1163 (82) | 257 (18) | 105 (7) | 38 (3) | 143 (10) | 223 (16) | 34 (2) | | pT3a | 743 (65) | 396 (35) | 130 (11) | 84 (7) | 241 (21) | 329 (29) | 67 (6) | | pT3b | 124 (46) | 144 (54) | 54 (20) | 50 (19) | 86 (32) | 100 (37) | 44 (16) | | Age at Dx, mean±SD, year | 62 ± 7 | 63 ± 7 | 63 ± 7 | 63 ± 6 | 62 ± 7 | 63 ± 7 | 63 ± 6 | | Pre-Rx PSA, median (IQR), ng/mL | 7 (5-9) | 8 (6-11) | 8 (6-12) | 9 (6-13) | 8 (6-11) | 8 (6-11) | 9 (6-13) | | Number of positive margin status core, median (IQR) | 3 (2-6) | 4 (2-7) | 5 (3-7) | 5 (3-7) | 4 (2-7) | 4 (2-6) | 5 (3-8) | | Tumour volume, median (IQR), cm3 | 2.3 (1.2-4.2) | 4.3 (2.3-8.3) | 4.6 (2.8-8.5) | 8.0 (3.3-12.7) | 4.0 (2.0-7.9) | 4.0 (2.2-7.7) | 7.6 (3.4-12.5) | | Nerve-sparing surgery, n (%)c | 1086 (53) | 420 (53) | 150 (10) | 71 (5) | 256 (17) | 354 (24) | 66 (4) |
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Cohort profile by margin statusa.
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| Factor | Any PSM | Apex | Bladder neck | Posterolateral | Multiple PSM sites | | OR | 95% CI | p-Value | OR | 95% CI | p-Value | OR | 95% CI | p-Value | OR | 95% CI | p-Value | OR | 95% CI | p-Value | | Age at diagnosis, year | | <60 | 1.0 | Reference | 0.76 | 1.0 | Reference | 0.61 | 1.0 | Reference | 0.94 | 1.00 | Reference | 0.09 | 1.0 | Reference | 0.41 | | 60-69 | 0.9 | 0.8-1.1 | 0.46 | 1.1 | 0.8-1.4 | 0.59 | 0.9 | 0.6-1.4 | 0.72 | 0.8 | 0.6-1.0 | 0.08 | 0.9 | 0.6-1.4 | 0.63 | | 70-79 | 1.0 | 0.7-1.3 | 0.75 | 1.1 | 0.7-1.7 | 0.66 | 1.0 | 0.6-1.7 | 0.93 | 0.7 | 0.5-1.1 | 0.10 | 0.7 | 0.4-1.4 | 0.34 | | Treatment period | | ≤2007 | 1.0 | Reference | 0.17 | 1.0 | Reference | 0.22 | 1.0 | Reference | 0.002 | 1.0 | Reference | 0.020 | 1.0 | Reference | 0.97 | | 2008-2010 | 1.0 | 0.8-1.2 | 0.79 | 0.7 | 0.5-1.0 | 0.06 | 2.0 | 1.1-3.5 | 0.020 | 1.0 | 0.8-1.4 | 0.810 | 1.0 | 0.6-1.7 | 0.98 | | 2011-2013 | 0.6 | 0.5-0.8 | 0.01 | 0.7 | 0.4-1.1 | 0.10 | 2.6 | 1.4-4.8 | 0.003 | 0.5 | 0.3-0.7 | <0.001 | 0.6 | 0.3-1.1 | 0.09 | | 2014-2016 | 0.8 | 0.6-1.2 | 0.31 | 0.7 | 0.4-1.1 | 0.15 | 3.1 | 1.7-5.9 | 0.001 | 0.7 | 0.5-1.1 | 0.140 | 1.2 | 0.6-2.1 | 0.63 | | Pre-treatment PSA, ng/mL | | <5 | 1.0 | Reference | 0.39 | 1.0 | Reference | 0.20 | 1.0 | Reference | 0.89 | 1.0 | Reference | 0.78 | 1.0 | Reference | 0.73 | | ≥5-<10 | 0.9 | 0.7-1.2 | 0.63 | 1.1 | 0.7-1.5 | 0.79 | 0.6 | 0.4-0.9 | 0.02 | 1.0 | 0.7-1.3 | 0.86 | 0.7 | 0.4-1.1 | 0.14 | | ≥10-20 | 1.3 | 0.9-1.7 | 0.08 | 1.7 | 1.1-2.6 | 0.02 | 0.9 | 0.5-1.5 | 0.73 | 1.2 | 0.9-1.7 | 0.25 | 1.4 | 0.8-2.5 | 0.22 | | ≥20 | 1.3 | 0.8-2.3 | 0.31 | 1.4 | 0.8-2.3 | 0.19 | 1.2 | 0.5-2.6 | 0.68 | 0.9 | 0.5-1.7 | 0.67 | 1.2 | 0.5-2.9 | 0.74 | | RP Gleason score | | ≤6 | 1.0 | Reference | 0.08 | 1.0 | Reference | 0.35 | 1.0 | Reference | 0.03 | 1.0 | Reference | 0.010 | 1.0 | Reference | 0.010 | | 3＋4 | 1.3 | 1.0-1.7 | 0.05 | 1.3 | 0.9-1.8 | 0.23 | 0.8 | 0.4-1.3 | 0.33 | 1.8 | 1.3-2.6 | <0.001 | 2.8 | 1.4-5.7 | 0.010 | | 4＋3 | 1.4 | 1.0-1.9 | 0.05 | 1.0 | 0.7-1.6 | 0.83 | 1.2 | 0.6-2.2 | 0.63 | 2.1 | 1.4-3.1 | <0.001 | 3.6 | 1.7-7.6 | 0.001 | | 8 | 1.5 | 0.9-2.3 | 0.10 | 1.3 | 0.7-2.5 | 0.36 | 1.7 | 0.8-3.7 | 0.17 | 2.1 | 1.2-3.5 | 0.006 | 4.9 | 2.0-11.4 | <0.001 | | 9-10 | 1.7 | 1.0-2.7 | 0.02 | 1.6 | 0.8-2.9 | 0.16 | 1.4 | 0.7-3.1 | 0.35 | 2.2 | 1.3-3.9 | 0.003 | 3.4 | 1.4-8.5 | 0.010 | | pT | | 2 | 1.0 | Reference | <0.001 | 1.0 | Reference | 0.01 | 1.0 | Reference | <0.001 | 1.0 | Reference | <0.001 | 1.0 | Reference | <0.001 | | 3a | 2.3 | 1.9-2.8 | <0.001 | 1.4 | 1.0-1.9 | 0.03 | 1.9 | 1.2-3.0 | 0.004 | 2.5 | 2.0-3.2 | <0.001 | 2.1 | 1.3-3.4 | 0.001 | | 3b | 3.4 | 2.5-4.7 | <0.001 | 1.9 | 1.2-2.8 | 0.003 | 3.4 | 2.0-5.8 | <0.001 | 3.4 | 2.4-4.9 | <0.001 | 4.0 | 2.3-7.0 | <0.001 | | Tumour volume, per 10 cm3 | | Q1 (≤1.4) | 1.0 | Reference | <0.001 | 1.0 | Reference | <0.001 | 1.0 | Reference | <0.001 | 1.0 | Reference | <0.001 | 1.0 | Reference | <0.001 | | Q2 (>1.4-2.7) | 1.3 | 0.9-1.9 | 0.10 | 2.3 | 1.2-4.5 | 0.01 | 2.1 | 0.8-5.6 | 0.14 | 1.2 | 0.8-1.7 | 0.47 | 2.3 | 0.7-7.2 | 0.170 | | Q3 (>2.7-5.4) | 1.7 | 1.2-2.5 | <0.001 | 3.7 | 2.2-7.5 | <0.001 | 3.0 | 1.2-7.6 | 0.02 | 0.9 | 0.6-1.4 | 0.62 | 1.7 | 0.5-5.5 | 0.380 | | Q4 (>5.4) | 2.9 | 2.0-4.0 | <0.001 | 5.3 | 2.8-9.9 | <0.001 | 8.9 | 3.7-20.4 | <0.001 | 1.5 | 1.0-2.3 | 0.05 | 7.8 | 2.5-20.6 | <0.001 | | Surgeon volumea | 0.93 | 0.88-0.98 | 0.004 | 0.96 | 0.89-1.03 | 0.26 | 0.90 | 0.82-0.97 | 0.010 | 0.91 | 0.87-0.97 | 0.003 | 0.85 | 0.76-0.95 | 0.003 | | Nerve-sparing surgery | 0.9 | 0.7-1.2 | 0.45 | 1.1 | 0.7-1.5 | 0.78 | 0.7 | 0.4-1.0 | 0.070 | 0.9 | 0.6-1.1 | 0.32 | 0.7 | 0.4-1.1 | 0.110 |
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Factors associated with any PSM, specific PSM sites, and multiple PSM sites derived from multivariable logistic regression models (1998-2016).
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Cumulative incidence plots with 95% confidence intervals by surgical margin status (any positive vs. negative). (A) Cumulative incidence of biochemical recurrence; (B) Cumulative incidence of second treatment; (C) Cumulative incidence of prostate cancer death.
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| Margin statusa | BCRb | Any secondary treatmentc | PCa deathd | | sHR | 95% CI | p-Value | sHR | 95% CI | p-Value | sHR | 95% CI | p-Value | | Any PSM vs. negative margin | 2.5 | 2.1-3.1 | <0.001 | 2.9 | 2.4-3.5 | <0.001 | 1.3 | 0.8-2.0 | 0.18 | | PSM at apex vs. all other casese | 1.7 | 1.3-2.2 | <0.001 | 2.0 | 1.6-2.5 | <0.001 | 1.3 | 0.7-2.4 | 0.39 | | PSM at bladder neck vs. all other casese | 1.9 | 1.4-2.5 | <0.001 | 1.8 | 1.3-2.5 | <0.001 | 1.7 | 0.9-3.5 | 0.11 | | PSM at posterolateral vs. all other casese | 2.1 | 1.7-2.5 | <0.001 | 2.3 | 1.9-2.8 | <0.001 | 0.9 | 0.6-1.6 | 0.83 | | Single PSM site vs. negative | 2.3 | 1.9-2.8 | <0.001 | 2.6 | 2.1-3.1 | <0.001 | 1.4 | 0.9-2.2 | 0.25 | | Multiple PSM sites vs. negative | 3.6 | 2.6-4.8 | <0.001 | 4.7 | 3.5-6.3 | <0.001 | 1.2 | 0.5-2.9 | 0.66 | | Intra-prostatic PSM vs. negativef | 4.5 | 3.2-6.3 | <0.001 | 4.8 | 3.3-7.0 | <0.001 | 0.8 | 0.3-2.2 | 0.59 |
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Risk of BCR, second treatment, and PCa mortality, associated with any PSM, PSM site, and multiplicity of sites, derived from competing risk regression models.
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| Margin status and pT | Relative to pT2 clear margin | PSM vs. clear margina | | sHR | 95% CI | p-Value | sHR | 95% CI | p-Value | | pT2 | | Clear margins | 1.0 | Reference | - | 1.0 | Reference | - | | Positive margin | 4.3 | 3.2-5.9 | <0.001 | 4.6 | 3.2-6.2 | <0.001 | | pT3a | | Clear margin | 2.2 | 1.7-2.9 | <0.001 | 1.0 | Reference | - | | Positive margin | 5.5 | 4.2-7.2 | <0.001 | 2.6 | 2.0-3.3 | <0.001 | | pT3b | | Clear margin | 4.9 | 3.4-7.0 | <0.001 | 1.0 | Reference | - | | Positive margin | 7.1 | 5.0-10.0 | <0.001 | 1.4 | 1.0-2.0 | 0.06 |
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Risk of biochemical recurrence by margin status and pT derived from competing risk regression models.
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