Abstract
BACKGROUND:
Analysis of systematic 12-core biopsies (SBx) has shown that African-American (AA) men tend to harbor higher risk prostate cancer (PCa) at presentation relative to other races. Multiparametric magnetic resonance imaging (mpMRI) and MRI-ultrasound fusion-guided biopsy (FBx) have been shown to diagnose more intermediate- and high-risk PCa in the general population; however, the efficacy in AA remains largely uncharacterized. We aim to evaluate the utility of FBx in an AA patient cohort.
METHODS:
Men suspected of PCa underwent an mpMRI and FBx with concurrent SBx from 2007 to 2015 in this institutional review board-approved prospective cohort study. Patient demographics, imaging and fusion biopsy variables were collected. χ2, Mann–Whitney U-test and McNemar’s tests were performed to compare proportions, means and paired variables, respectively. Clinically significant PCa (CSPCa) was defined as Gleason score ≥ 3+4.
RESULTS:
Fusion biopsy demonstrated exact agreement with SBx risk categories in 64% of AA men. There was no statistically significant difference in the detection of CSPCa between FBx vs SBx (68 vs 62 cases, P = 0.36). However, FBx detected 41% fewer cases of clinically insignificant PCa (CIPCa) compared with SBx (FBx 30 vs SBx 51 cases, P = 0.0004). The combined FBx/SBx biopsy approach detected significantly more cases of CSPCa (FBx/SBx 80 vs SBx 62 cases, P = 0.004) while detecting comparable number of cases of CIPCa (FBx/SBx 45 vs SBx 51 cases, P = 0.37) compared with SBx alone. FBx/SBx also detected more CSPCa in patients with a history of prior negative SBx (FBx/SBx 28 vs 19 cases, P = 0.003).
CONCLUSIONS:
FBx when used in combination with SBx detected more cases of CSPCa while not significantly increasing the diagnosis of CIPCa in AA men. Future multicenter studies will be needed to validate ultimately the clinical implications of FBx in AA patients.
INTRODUCTION
African-American (AA) race1,2 is a major risk factor for prostate cancer (PCa) with United States’ AA men reported to have the highest incidence3,4 of PCa among all races. At initial presentation, AA men tend to have higher Gleason score (GS), more advanced disease and are more likely to do poorly with treatment.5 Robust screening measures (PSA, digital rectal exam) have led to the diagnosis of more organ-confined disease, but incidence and mortality in AAs remain disproportionately high and relatively unchanged.6
Multiparametric magnetic resonance imaging (mpMRI) and MRI-ultrasound fusion-guided biopsy (FBx) are novel diagnostic techniques that have been shown to diagnose more high-risk PCa and fewer cases of low-risk PCa in the general population compared with the systematic 12-core biopsy (SBx).7 While the current trend of evidence projects a near-future incorporation of FBx as a major clinical diagnostic tool for PCa, the efficacy of this approach within the AA population remains largely uncharacterized.8,9 Given the tendency for higher risk disease in AA men, we sought to determine whether mpMRI and FBx confer a similar benefit in this population.
MATERIALS AND METHODS
Patient enrollment
Patients were enrolled (from 2007 to 2015) in an institutional review board-approved prospective trial on the use of an electromagnetic tracking in targeting PCa lesions. Patients with elevated PSA or abnormal digital rectal exam, and found with at least one suspicious mpMRI lesion, were included in the study.
Imaging protocol
All patients underwent an mpMRI on a 3.0 T MRI Scanner (Achieva; Phillips Healthcare, Best, Netherlands) as described previously.10 Three sequences (T2-weighted image, dynamic contrast enhancement and diffusion-weighted images) were used to analyze suspicious prostate lesions. These image sequences were acquired using an endorectal coil (BPX, 30 Medrad) and a 16-channel surface coil (SENSE; Phillips Healthcare). Two highly experienced (9 and 15 years of interpreting prostate mpMRI) genitourinary radiologists analyzed the images and each lesion was assigned a suspicion score (low, intermediate or high) that predicts its likelihood for cancer. These scores were based on lesion characteristics on all three-image sequences as described.8,11 The majority of the enrollment period preceded the introduction of the currently standardized Prostate Imaging Reporting And Data System criteria,12 and thus the original scoring system was used across the entire cohort for consistency.
Biopsy protocol
The mpMRI images with suspicious lesions were subsequently segmented and biopsy target points were created based on lesion location (DynaCAD; Invivo, Gainsville, FL, USA). One physician performed FBx followed by SBx in the same procedure session performed by another physician (blinded to the mpMRI findings). Using the UroNav MR/Ultrasound fusion device (Phillips Medical/Invivo), lesions were targeted using T2-weighted image coregistered with real-time transrectal ultrasound images. Each lesion was targeted in the axial and sagittal planes yielding 2 cores per lesion. SBx involved the collection of 12 cores in an extended-sextant template. A single genitourinary pathologist reviewed all pathology specimens.
Data analysis
All data were prospectively collected and managed by a dedicated data manager. Patients were risk categorized into low, intermediate or high based on biopsy findings. Low risk was defined as GS 3+3, intermediate risk as 3+4 and 4+3 and high risk as >4+3. GS sum >6 was considered clinically significant PCa (CSPCa). Overall gland Gleason (or risk category) was determined by the highest GS (if there were more than one tumor detected).
Statistical analysis
R statistics package and JMP were used for the statistical analysis. Wilcoxon’s rank-sum test was used to compare distribution of continuous variables (PSA, age, prostate volume and so on) within categories (AA vs white/Other, prior biopsy vs no prior biopsy and so on). Fisher’s exact test was used to compare proportions (risk categories) between biopsy modalities (SBx vs FBx) and race (AA versus white/Other). McNemars test was used to compare paired variables (CSPCa vs no CSPCa) between SBx and FBx.
RESULTS
A total of 1262 (195 AA and 1067 W/O) patients underwent mpMRI and subsequent FBx with concurrent SBx during the same session. Patient demographics are listed in Table 1.
Table 1.
Patient demographics
| Variable | Entire cohort | AA | W/O | aP-value |
|---|---|---|---|---|
| No. of men (% of total) | 1262 | 195 (15.5) | 1067 (84.5) | |
| Mean age, years, (± s.d.) | 62.2 ±8.4 | 60.3 ± 8.6 | 62.6 ± 8.4 | 0.0005 |
| Median PSA (ng/ml; IQR) | 6.6 (4.4–10.4) | 7.8 (5.1–12) | 6 (4.2–10) | 0.002 |
| Median MRI prostate volume (cm3) (IQR) | 49 (36–69) | 49 (36–72) | 49 (37–69) | 0.84 |
| Positive family history, no. (%) | 366/1195 (30.6) | 85/187 (45.5) | 281/1008 (27.9) | < 0.0001 |
| Smoking history, no. (%) | 184/1201 (15.3) | 54/188 (28.7) | 130/1013 (12.8) | < 0.0001 |
| BMI | 28.1 ± 4.3 | 29.3 ± 4.2 | 27.7 ± 4.3 | < 0.0001 |
| Tumor staging, no. (%) | ||||
| T1c | 1194 (95) | 191 (98) | 1003 (94) | |
| T2a | 61 (5) | 4 (2) | 57 (5.4) | |
| T2b | 3 (0.2) | 0 (0) | 3 (0.3) | |
| T2c | 2 (0.15) | 0 (0) | 2 (0.2) | |
Abbreviations: AA, African American; BMI, basic metabolic index; IQR, interquartile range; MRI, magnetic resonance imaging; W/O, white/other.
P-value for comparison of AA versus W/O.
Fusion biopsy demonstrated exact agreement with SBx risk categories in 64% (125/195) of AA (Table 2; green). SBx diagnosed more cases of cancer compared with FBx (SBx: 113 vs FBx: 98 cases, P = 0.025); however, many of these were clinically insignificant PCa (CIPCa) (SBx: 51 vs FBx 30 cases). In cases where SBx detected CSPCa in AA men, there was poor risk category agreement (35/62, 56.5%) between SBx and FBx leaving 43.5% of the CSPCa cases at risk of misclassification if SBx was carried out alone.
Table 2.
Comparison of MR/US fusion and systematic 12-core biopsy Gleason scores in the AA patient cohort
| AA |
MR/US fusion |
Total | ||||
|---|---|---|---|---|---|---|
| No cancer | Low risk | Intermediate risk | High risk | |||
| Systematic 12-core | 3+3 | 3+4 | 4+3 | >4+3 | ||
| No cancer | 70 | 3 | 3 | 1 | 5 | 82 |
| Low risk | ||||||
| 3+3 | 21 | 21 | 5 | 1 | 3 | 51 |
| Intermediate risk | ||||||
| 3+4 | 5 | 6 | 16 | 3 | 6 | 36 |
| 4+3 | 1 | 0 | 0 | 3 | 2 | 6 |
| High risk | ||||||
| >4+3 | 0 | 0 | 3 | 1 | 16 | 20 |
| Total | 97 | 30 | 27 | 9 | 32 | 195 |
Abbreviations: AA, African American; MRI, magnetic resonance imaging; US, ultrasound; W/O, white/other.
Fusion biopsy detected 41% (AA: FBx 30 vs SBx 51 cases, P = 0.0004) fewer cases of CIPCa and 10% (AA: FBx 68 vs SBx 62 cases, P = 0.36) more cases of CSPCa compared with SBx. When FBx demonstrated a higher risk category, 29/68 (42.6% AA; Table 2, orange) were upgraded to intermediate- or high-risk pathology by FBx from SBx.
In Table 3, overall cancer detection rate (CDR) of combined (FBx/SBx) biopsy approach was higher in AA (64.1%) than in W/O (56.7%), P = 0.08. Combined FBx/SBx demonstrated increased detection of CSPCa (GS >3+3) compared with SBx alone in AA (CDR: FBx/SBx 80 vs SBx 62 cases, P = 0.004). Of the 18 additional CSPCa cases detected by the combined biopsy approach, 12 (66.7%) harbored anterior prostate lesions on MRI. On the other hand, combined FBx/SBx did not show significant difference in the detection of CIPCa in AA (CDR: FBx/SBx 45 vs SBx 51 cases, P = 0.37) compared with SBx alone. Assessing CDR based on prior biopsy history, FBx/SBx detected more overall cancer (FBx/SBx 46 vs SBx 38 cases, P = 0.004) and CSPCa (FBx/SBx 28 vs SBx 19 cases, P = 0.003) compared with SBx alone in the prior negative biopsy patient cohort. No biopsy approach significantly detected more overall cancer or CSPCa in the biopsy-naïve patient cohort (Table 4).
Table 3.
Patient biopsy characteristics
| Variable | Entire cohort | AA | W/O | aP-value |
|---|---|---|---|---|
| Combined SBx/FBx CDR (%) | 730 (57.8) | 125 (64.1) | 605 (56.7) | 0.08 |
| Systematic 12-core CDR (%) | 608 (48.2) | 113 (57.9) | 495 (46.4) | 0.005 |
| Fusion biopsy CDR (%) | 588 (46.6) | 98 (50.3) | 490 (45.9) | 0.31 |
| Prior negative biopsy, no. (%) | 561/1021 (54.9) | 94/165 (57.0) | 467/856 (54.6) | 0.61 |
| Prior biopsy history (SBx) | 0.27 | |||
| Biopsy naïve | 241 | 30 | 211 | |
| Biopsy positive | 460 | 71 | 389 | |
| Biopsy negative | 561 | 94 | 467 | |
| No. of FBx cores per patient, mean | 5.1 ± 2.1 | 5 ± 2.6 | 5.2 ± 2.5 | |
| No. of SBx cores, per patient, mean | 12.2 ± 0.6 | 12.2 ± 0.5 | 12.2 ± 0.6 | |
| Patients with anterior prostate lesions, no. (%) | 584 (46.1) | 93 (47.7) | 491 (45.8) | 0.63 |
| No anterior lesions, no. | 720 | 109 | 611 | |
Abbreviations: AA, African American; CDR, cancer detection rate; FBx, fusion biopsy; PCa, prostate cancer; SBx, systematic 12-core biopsy; W/O, white/other.
P-value for comparison of AA versus W/O.
Table 4.
Prior negative biopsy and biopsy naive cancer detection rates
| Variable | Prior negative (n = 94) | P-value | Biopsy naïve (n = 30) | P-value |
|---|---|---|---|---|
| Overall CDR | ||||
| Systematic 12-core CDR (%) | 38 (40.4) | Ref. | 26 (86.7) | Ref. |
| Fusion biopsy CDR (%) | 36 (38.3) | 0.41 | 23 (76.7) | 0.50 |
| Combined SBx/FBx CDR (%) | 46 (48.9) | 0.004 | 24 (80.0) | 0.25 |
| CDR of clinically significant PCa | ||||
| Systematic 12-core CDR (%) | 19 (20.2) | Ref. | 16 (53.3) | Ref. |
| Fusion biopsy CDR (%) | 24 (25.5) | 0.17 | 16 (53.3) | 0.99 |
| Combined SBx/FBx CDR (%) | 28 (29.9) | 0.003 | 20 (66.7) | 0.05 |
Abbreviations: CDR, cancer detection rate; FBx, fusion biopsy; PCa, prostate cancer; SBx, systematic 12-core biopsy.
DISCUSSION
In this study, we sought to evaluate if FBx confers a similar benefit in cancer detection for AA men who more often present with intermediate- or high-risk PCa.5,13–15 The benefit of FBx alone in detecting CSPCa (10% more cases) in our AA cohort was marginally compared with the benefit reported by Siddiqui et al.7 (30% more cases) in a more general patient population. Shin et al.,16 in a smaller study of 117 AA men, shows FBx to significantly detect more CSPCa compared SBx (52.9 vs 12.4 P < 0.001).16 While Shin et al.’s16 results do not contradict our findings, they illustrate the need for larger high-powered multi-institutional studies in the future that will further validate and generalize these conclusions.
Despite the marginal benefit of FBx in detecting CSPCa, combined FBx/SBx, however, demonstrated superior performance in CDR of CSPCa compared with SBx alone. The added increase in CDR of CSPCa by combined biopsy approach, despite similar individual CDRs, indicates detection of PCa missed by either biopsy technique alone. We note FBx to miss 12 (6.2%) cases of CSPCa in this patient cohort. This number is similar to that reported (6.2%) in a study by Muthigi et al.,17 which found 6.2% (62/1003) of the CSPCa cases to be upgrades by SBx of FBx.17 They allude to four possible mechanisms of failure of FBx: radiologist oversight, MR invisible lesions, inaccurate sampling due to registration/mechanical error and lesion heterogeneity. In regards to the added number of CSPCa in the combined biopsy approach, we note a significant number of these cases to harbor anterior MRI lesions. Anterior sampling by FBx gives the combined biopsy approach a greater chance of detecting anterior cancers, which would otherwise be missed by the peripheral zone-focused sampling of SBx.18 Generally, FBx involves selective targeting of areas within the prostate found to be highly suspicious rather than random sampling of regions of the prostate.19 At this time, pending a larger cohort study, we recommend a combination of FBx and SBx in the AA population.
Prior negative SBx patients had a significantly higher CDR with the combined biopsy approach but not with FBx compared with SBx. Consensus statements based on a host of studies show FBx to detect more CSPCa compared with SBx in prior negative biopsy patients.20 It is unclear why FBx does not show similar results in our AA cohort, but the small sample size remains a major limitation to making strong conclusions about our findings. At this point in time, we therefore would not recommend a FBx only approach in AA men with prior negative SBx.
Fusion biopsy alone detected fewer cases of CIPCa in the AA cohort. This was consistent with the already reported low detection rate of CIPCa by FBx in the general population.7,21 Theoretically, this finding could potentially reduce overtreatment of CIPCa. Decreased detection of CIPCa is one potential approach to addressing overdiagnosis/overtreatment. There has been an overutilization of radical treatment (radiation, surgery) of CIPCa over active surveillance, although with longitudinal follow-up its adoption has been increasing.22,23 One could also argue that decreased detection of CIPCa by FBx alone may be detrimental as low-risk cancers have been shown to progress into more aggressive cancers during active surveillance in AA men at a higher rate compared with Caucasian men.24 This again emphasizes the need for a combined FBx/SBx biopsy approach in AA men at this point in time.
SBx of the prostate detected significantly more PCa in our AA cohort than it did in other races. Further analysis showed that SBx detected more CIPCa in this cohort, a concern for overtreatment. Misclassification of PCa by SBx is one of the major concerns of current disease management. As many as 54% of PCa cases could be misclassified by SBx25,26 alone. Although SBx did not miss a significant amount of CSPCa, agreement with FBx was poor leaving a significant number of cases at risk for misclassification. FBx has been shown to accurately risk stratify PCa27,28 and could be used in AAs for proper risk stratification pending validation in a larger patient cohort.
Our study is not without its limitations. Although patient accrual was prospective, our study was retrospective in nature and therefore possesses inherent bias associated with this type of study. In addition, the study population consisted of patients referred to a single institution introducing potential selection bias. Also, our institution is a center of excellence in mpMRI and FBx and our results may not be reproducible in small community centers; however, 31.3% of FBx are currently being performed by community centers.29 Furthermore, the AA vs W/O comparison data was not generated from a matched cohort; however, the focus of this study is on AA men and not on an AA vs W/O comparative analysis. Last, the AA study population was small and future multicenter studies will allow for a better understanding of the benefits of FBx in this patient population.
CONCLUSION
All in all, FBx when used in combination with SBx detected more CSPCa while not significantly increasing the diagnosis CIPCa. Future multicenter studies will be needed to validate ultimately the clinical implications of FBx in AA patients.
ACKNOWLEDGEMENTS
We would like to acknowledge our data managers who prospectively maintain our databases.
Footnotes
CONFLICT OF INTEREST
The authors declare no conflict of interest.
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