Cancer Detection Rate of MRI Ultrasound Fusion Prostate Biopsy in 1,039 Patients and Number Needed to Biopsy in Rargeted Lesion


Sivakorn Choomark, M.D., Pubordee Aussavavirojekul, M.D., Varat Woranisarakul, M.D., Sittiporn Srinualnad, M.D.

Division of Urology, Department of Surgery, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand.


ABSTRACT

Objective: To determine the cancer detection rate (CDR) of magnetic resonance imaging ultrasound fusion prostate biopsy (MRI/US fusion prostate biopsy) in Thailand. The secondary aim was to estimate the number needed to biopsy (NNB) for each prostate lesion in a targeted biopsy, classified by Prostate Imaging-Reporting and Data System (PI-RADS).

Materials and Methods: The data of 1,039 consecutive patients who underwent a MRI/US fusion prostate biopsy at Siriraj Hospital between September 2017 and February 2021 was included and retrospectively reviewed. Those included had previous negative biopsies and were biopsy naïve. The data was analyzed to find the detection rate and NNB.

Results: The overall detection rate of MRI/US fusion prostate biopsy was 58.71%, whereas that of systematic biopsy was 45.72%. Clinically significant prostate cancer (csPCa) (Gleason score ≥ 3+4) detection rate of MRI/US fusion prostate biopsy was 51.01%. When categorized by PI-RADS category 3, 4, and 5 were 12.16%, 44.98%, 85.71% respectively. NNB in targeted biopsy of PI-RADS 3, 4, and 5 were 8, 7, and 3 times sequentially. Positive predictive factors for prostate cancer (PCa) detection were age, prostate-specific antigen density (PSAD) and PI-RADS, whereas prostate volume was a negative predictive factor.

Conclusion: This study supports the role of MRI/US fusion prostate biopsy in PCa detection and should not avoid systematic biopsies. The higher the PI-RADS was, the greater the csPCa detection rate. NNB is helpful in guiding the least amount of biopsied cores for each lesion.

Keywords: Cancer detection rate, Magnetic resonance imaging ultrasound fusion prostate biopsy, Number needed to biopsy, PI-RADS score, Gleason score (Siriraj Med J 2023; 75: 770-777)


INTRODUCTION

Prostate cancer (PCa) is the third most common malignancy diagnosed1, and is the eighth cause of cancer death in the world.2 Thai guidelines for PCa screening recommend a prostate specific antigen (PSA) and digital rectal examination (DRE) screening in men aged 50-75, with at least 10 years of estimated life expectancy, and at the age of 45 and older in men with a family history of

PCa. A prostate biopsy is indicated when any of the two investigation above are flagged as abnormal. Currently, prostate biopsies are widely performed following the transrectal ultrasound guided biopsy technique (TRUS biopsy) and 12-cores systematic biopsy strategy. Afterwards, obtained tissues are stained and examined by pathologists. Although it is a frequently used method, the cancer detection rate (CDR) of this method is about 44.4%.3


Corresponding author: Sittiporn Srinualnad E-mail: sitsrinualnad@gmail.com

Received 15 September 2023 Revised 9 October 2023 Accepted 10 October 2023 ORCID ID:http://orcid.org/0000-0002-5118-7675 https://doi.org/10.33192/smj.v75i11.265361


All material is licensed under terms of the Creative Commons Attribution 4.0 International (CC-BY-NC-ND 4.0) license unless otherwise stated.

The hypothesis of this study is that magnetic resonance imaging ultrasound fusion prostate biopsy (MRI/US fusion prostate biopsy) may be the key to improving the prostate detection rate. Currently, multiparametric magnetic resonance imaging (mpMRI) is the most interesting method utilized for identifying the presence of any suspicious lesions within the prostate. Suspicious lesions were classified into five categories, according to the Prostate Imaging-Reporting and Data System (PI- RADS), and ranged from 1 (no suspicious lesions visible) to 5 (aggressive lesion appearance which is resemble cancer).

As modern imaging technologies allow region of interest (ROI) for cancer become identifiable, numerous biopsy methods are proposed such as cognitive-target biopsy and in-bore MRI guided biopsy. Later, the MRI/US fusion prostate biopsy method was created to overcome inaccuracy problems as it provided real-time lesion tracking and required less effort and hassle.4 Since 2017, MRI/ US fusion prostate biopsies have become the preferred method of urologists at Siriraj Hospital.

Many studies5-7 classified PCa into two categories; clinically insignificant prostate cancer (ciPCa) and clinically significant prostate cancer (csPCa). ciPCa is usually an organ-confined disease while csPCa often manifests as a non-organ-confined disease.8 This study intended to report the CDR of MRI/US fusion prostate biopsies for overall and csPCa at our institute. It also proposed the estimated numbers required for a biopsy for each visible lesion targeted, as classified by the PI-RADS.


MATERIALS AND METHODS

Patients who underwent a MRI/US fusion prostate biopsy between September 2017 and February 2021 were included. All cases had at least one PI-RADS 3 lesion in the multiparametric magnetic resonance imaging (mpMRI) and underwent a MRI/US fusion prostate biopsy, targeted and systematic. Patients under active surveillance protocol, previous diagnosis of PCa, or those who had a radical prostatectomy or incomplete data were excluded. A total of 1,039 patients were eligible for this study. Patients’ demographic data, urological history, DRE, PSA, MRI reports, operative notes, pathological reports, and post-operative complications were collected and analyzed.


Imaging

The mpMRI of the prostate in this study was performed with a 1.5 or 3 Tesla, without endorectal coil. The imaging protocol consisted of T2-weighted imaging, diffusion-weighted imaging (DWI) and apparent

diffusion coefficient (ADC) value. Radiologists reported lesions within the prostate according to the PI-RADS.

Intervention

Most patients in this study were admitted one day prior to the operation. Only a few operations were performed as a one-day surgery. The trans-perineal biopsy approach was the preferred option of most surgeons, and thus, general anesthesia was almost always used to ensure adequate pain control. After a patient was under anesthesia, he was placed in the standard lithotomy position. Catheter placement wasn’t mandatory and the decision was left to the surgeon. A MRI/US fusion prostate biopsy device, known as KOELIS TrinityÒ system (Koelis, France), was brought in to map current ultrasonographic images with MRI. After each lesion was identified, a targeted biopsy was performed, lesion by lesion, according to the guidance by systematic biopsy in a free-hand manner. Following the operation, patients were observed in the recovery room for two hours before transfer to the ward or discharge. In most cases, patients were discharged within one day of the operation unless they experienced complications.

Systematic biopsy was random biopsy that obtained tissue from both sides of prostate including the prostatic base, mid gland and apex.7 Targeted biopsy was biopsy at the positive lesions on MRI (PI-RADS 3, 4, 5) with the use of MRI/US fusion prostate biopsy device to obtain tissue from regions of interest. Combination was MRI/ US fusion prostate biopsy including both systematic and targeted biopsy.


Histology

Histopathological tissues were interpreted and reported by assigned pathologists within Siriraj Hospital using the International Society of Urological Pathology (ISUP) consensus definition of Gleason score (GS) and Grade groups (GG). A csPCa was defined as GS ≥ 3+4 or GG ≥ 2, and ciPCa was GS 3+3 or GG 1.7,9,10


Number needed to biopsy

The number needed to biopsy (NNB) was calculated by dividing the total number of biopsies of a particular prostate lesion by the number of positive prostate cancer biopsies. We modified the NNB from the NNB ratio to diagnose s melanoma (Marchetti et al).11 We excluded patients with a benign pathology report and patients with multiple lesions within the prostate in this analysis. A single PI-RADS lesions represented specific patients and lesions and could be properly interpreted. The cumulative line plot of NNB was used to demonstrate cancer detection

yield for each additional biopsy core in each PI-RADS category.

Statistical analysis

The statistical analysis of this study was performed using Python (Python Software Foundation, Wilmington, DE, USA). Univariate and multivariate analyses were performed using linear regression and multiple linear regressions via the package statsmodels version 0.12.0. A p-value less than 0.05 was considered statistically significant difference.


RESULTS

Demographic data from 1,039 patients in this study revealed a median age of 69 (64.5-75), median PSA of

8.79 ng/mL (6.29-13.7), median prostate volume of

44.06 mL (29.9-63.6), median PSAD of 0.21 ng/mL2 (0.14-0.34), and median maximal lesion diameter of 13 mm (9-19) (Table 1). Among the biopsied patients, there were 264 instances of previous negative biopsies and 775 biopsy-naïve cases. Most patients in both groups were PI-RADS 4 patients. The presence of PI-RADS 3 patients in each group was less common. A total of 659 patients (63.43%) had one visible lesion in the mpMRI. Another 301 patients (28.97%) had two ROI. There was also one pers on who had a total of six lesions within the prostate, representing the highest number of lesions in a single patient in this study (Table 2). This study revealed overall and csPCa detection rate of MRI/US fusion prostate biopsy of 58.71% and 51.01%, respectively.

Fig 1 presents the proportion of different cell types found in suspicious lesions, categorized by the MRI findings. The patients with PI-RADS 5, which exhibited the most aggressive features in mpMRI, had highest detection rate for significant cancer at 85.71%. The CDR for csPCa in PI-RADS 4 and 3 were 44.98%, and 12.16% respectively. In PI-RADS 5, the most frequent highest GS was 4+5, or 27.47%, followed by 4+3 and 3+4 or 19.78% each, respectively. On the other hand, PI-RADS 3 and 4 mainly consisted of ciPCa or benign outcomes (GS 6 or lower) at 87.84% and 55.02%, respectively. The most frequent csPCa in PI-RADS 3 and 4 was a GS of 3+4 (4.05%, 23.62%) sequentially (Table 2). In this study, common complications in the first 14 days after biopsy were acute urinary retention (AUR) at 4.33%, and gross hematuria (GH) at 2.98%, however, sepsis was zero.

Regarding the Venn diagram in Fig 2, PCa was mostly found in both targeted core tissues and systematic core tissues, or in 409 patients (39.37%). Another 135 patients (12.99%) with a positive result in targeted biopsy tissue represented the edge of the MRI/US fusion technique over the systematic biopsy strategy. In contrast, 66 patients (6.35%) had infiltrative tumors, which were invisible on mpMRI and were only found by a systematic biopsy. About half of this group, or 34 patients, were diagnosed with csPCa. The rest, or 429 patients (41.29%), tested negative for PCa.

Univariate and multivariate analyses in Table 3 identified significant predictors, which were similar in outcomes. Age, PSAD, prostate volume, and PI-RADS



TABLE 1. Characteristics of 1,039 patients who underwent MRI/US fusion prostate biopsy.




Characteristics

Total

(N=1,039)

PIRADS 5

(n=273, 26.28%)

PIRADS 4

(n=618, 59.48%)

PIRADS 3

(n=148, 14.24%)

Age (years)a

69 (64.50 - 75.00)

71 (67.00-77.00)

69 (64.25 - 74.00)

67 (62.00 - 72.00)

PSA (ng/mL)a

8.79 (6.29 - 13.70)

12 (7.74 - 20.16)

7.8 (5.85 - 11.36)

9.45 (6.49 - 14.26)

MRI-Prostate volume (g)a

44.06 (29.90 - 63.60)

37.75 (26.95 - 55.68)

44.95 (30.80 - 63.70)

55.6 (36.67 - 70.62)

PSAD (ng/mL2)a

0.21 (0.14 - 0.34)

0.34 (0.20 - 0.59)

0.18 (0.12 - 0.27)

0.19 (0.12 - 0.28)

Maximum total sizea

13 (9.00 - 19 .00)

20 (17.00 - 26.00)

11 (8.00 - 14.00)

11 (8.00 - 15.00)

Biopsy Naïveb

775 (74.59)

213 (78.02)

457 (73.95)

105 (70.95)

Previous negative biopsyb

264 (25.41)

60 (21.98)

161 (26.05)

43 (29.05)

a Data are presented as median (interquartile range)

b Data are presented as n (%)



TABLE 2. MRI lesion and MRI/US fusion prostate biopsy outcomes of 1,039 patients.



Total

PI-RADS 5

PI-RADS 4

PI-RADS 3

(N=1,039)

(n=273)

(n=618)

(n=148)

MRI (lesion)





1 659 (63.43)

167 (61.17)

389 (62.94)

103 (69.59)


2 301 (28.97)

80 (29.30)

180 (29.13)

41 (27.70)


3 58 (5.58)

20 (7.33)

34 (5.50)

4 (2.70)


4 17 (1.64)

3 (1.10)

14 (2.27)

0


5 3 (0.29)

2 (0.73)

1 (0.16)

0


6 1 (0.10)

1 (0.37)

0

0


Single lesion

659 (63.43)

167 (61.17)

389 (62.94)

103 (69.59)

Multiple lesion

380 (36.57)

106 (38.83)

229 (37.06)

45 (30.41)

MRI/US fusion prostate biopsy





Gleason score





<3+3

429 (41.29)

32 (11.72)

281 (45.47)

116 (78.38)

3+3

80 (7.70)

7 (2.56)

59 (9.55)

14 (9.46)

3+4

206 (19.83)

54 (19.78)

146 (23.62)

6 (4.05)

4+3

118 (11.36)

54 (19.78)

58 (9.39)

6 (4.05)

4+4

55 (5.29)

30 (10.99)

23 (3.72)

2 (1.35)

3+5

13 (1.25)

6 (2.20)

7 (1.13)

0

5+3

3 (0.29)

0

3 (0.49)

0

4+5

115 (11.07)

75 (27.47)

36 (5.83)

4 (2.70)

5+4

15 (1.44)

11 (4.03)

4 (0.65)

0

5+5

5 (0.48)

4 (1.47)

1 (0.16)

0



Detection rates

100%

90%

12.16%

80%

70%

60%

9.46%

51.01%

44.98%

85.71%

50%

9.55%

7.70%

40%

78.38%

csPCa ciPCa

Benign

30%

20%

10%

0%

41.29%

45.47%

2.57%

11.72%

Total PI-RADS 5 PI-RADS 4 PI-RADS 3

(N = 1039) (n = 273) (n = 618) (n = 148)

Fig 1. Cancer detection rate of MRI/US fusion prostate biopsy of 1,039 patients. Clinical insignificant prostate cancer (ciPCa): GS 3+3 or GG 1,

Clinically significant prostate cancer (csPCa): GS ≥ 3+4 or GG ≥ 2

Choomark et al.




TABLE 3. Univariate and multivariate analysis in csPCa and overall cancer.




csPCa outcome Univariate analysis



Multivariate analysis

Any cancer outcome Univariate analysis


Multivariate analysis


OR (95% CI)

P-value

OR (95% CI) P-value

OR (95% CI) P-value

OR (95% CI)

P-value

Age (years) <60

1 (ref)


1 (ref)

1 (ref)

1 (ref)


61 to 80

1.81 (1.15, 2.86)

0.011

2.45 (1.40,4.26) 0.002

1.54 (0.99,2.39) 0.055

1.94 (1.14,3.32)

0.014

>80

5.04 (2.51, 10.18)

<0.001

4.24 (1.80,9.97) 0.001

4.07 (1.97,8.41) <0.001

3.3 (1.40,7.77)

0.006

PSA (ng/mL) <4

1 (ref)


1 (ref)

1 (ref)

1 (ref)


4 to 10

1.73 (0.86, 3.46)

0.123

1.14 (0.50,2.61) 0.749

1.93 (0.98,3.82) 0.056

1.34 (0.61,2.97)

0.464

>10

2.40 (1.19, 4.85)

0.014

0.95 (0.36,2.51) 0.925

2.54 (1.28,5.05) 0.008

1.11 (0.44,2.83)

0.821

PSAD (ng/mL2) <0.15

1 (ref)


1 (ref)




0.15 to 0.30

2.17 (1.60, 2.94)

<0.001

1.86 (1.22,2.83) 0.004

2.35 (1.75,3.19) <0.001

2.01 (1.35,3.00)

0.001

>0.30

7.00 (4.95, 9.87)

<0.001

3.89 (2.18,7.17) <0.001

6.78 (4.76,9.68) <0.001

3.68 (2.01,6.69)

<0.001

Prostate <30

1 (ref)


1 (ref)

1 (ref)

1 (ref)


Volume (g) 30 to 50

0.51 (0.36, 0.71)

<0.001

0.63 (0.41,0.97) 0.036

0.49 (0.34,0.71) <0.001

0.61 (0.39,0.95)

0.03

>50

0.21 (0.15, 0.30)

<0.001

0.39 (0.23,0.66) <0.001

0.21 (0.14,0.29) <0.001

0.37 (0.22,0.64)

<0.001

Average targeted ≤6

1 (ref)


1 (ref)

1(ref)

1 (ref)


core biopsy 7 to 10

1.48 (1.12, 1.93)

0.006

1.06 (0.76,1.49) 0.73

1.4 (1.06,1.84) 0.018

1.06 (0.76,1.48)

0.72

per lesion >10

2.02 (1.45, 2.83)

<0.001

1.19 (0.78,1.82) 0.421

1.94 (1.36,2.75) <0.001

1.23 (0.80,1.88)

0.34

PI-RADS MPI-RADS 3

1 (ref)


1 (ref)

1 (ref)

1 (ref)


SPI-RADS 3

0.86 (0.30, 2.46)

0.773

0.85 (0.28,2.53) 0.764

0.95 (0.41,2.23) 0.907

0.93 (0.38,2.27)

0.876

MPI-RADS 4

4.61 (1.88, 11.36)

0.001

4.68 (1.77,12.30) 0.002

4.06 (1.92,8.58) <0.001

4.37 (1.90,9.97)

<0.001

SPI-RADS 4

5.83 (2.41, 14.15)

<0.001

5.59 (2.20,14.15) <0.001

4.33 (2.08,9.03) <0.001

4.07 (1.86,8.84)

<0.001

MPI-RADS 5

34.03 (12.43, 92.76)

<0.001

22.34 (7.39,67.36) <0.001

25.04 (10.07,62.18) <0.001

17.00 (6.17,46.99)

<0.001

SPI-RADS 5

42.55 (16.12, 112.17)

<0.001

32.26 (11.59,90.02) <0.001

27.08 (11.59,63.43) <0.001

19.71 (8.00,48.91)

<0.001

Surgeon Staff

1 (ref)



1 (ref)



2nd-year residents

0.91 (0.51, 1.60)

0.732


0.8 (0.45,1.42) 0.454



3rd-year residents

0.77 (0.52, 1.13)

0.174


0.81 (0.55,1.19) 0.283



4th-year residents

1.08 (0.80, 1.46)

0.605


0.89 (0.66,1.21) 0.461



Abbreviations: MPI-RADS: multiple lesion PI-RADS, SPI-RADS: single lesion PI-RADS




NNB = 3

NNB = 7

NNB = 8

Fig 3. Number needed to biopsy (NNB) in each PI-RADS at the 95th Percentile

Fig 2. Venn diagram of MRI/US fusion prostate biopsy of 1,039 patients.


category were significant independent predictors regarding multivariate analyses, whereas prostate volume was the only negative predictor. PSA and average targeted core biopsy per lesion remained significant in univariate analyses, but multivariate analyses suggested otherwise due to their dependency on other factors. Surgeon experience proved to be insignificant regarding CDR when performed by second, third, and fourth postgraduate year residents and also board-certified urologists.

Of a total of 1,039 patients, 292 were eligible for the calculation of NNB, as they had a single lesion in MRI results and were diagnosed with PCa after a biopsy. According to Fig 3, the cumulative plot illustrates an increasing yield of cancer detection in each additional core in targeted biopsies regarding calculated NNBs. For PI-RADS 4 and 5 lesions, 7 and 3 were recommended as the minimum cores, as the curves reached the plateau approximately at 95% yield of cancer detection. In contrast, the number of eligible patients in PI-RADS 3 group was relatively too low to assure 95% yield at the minimum of 8 cores.

DISCUSSION

According to NCCN Guidelines Version 1.2023, mpMRI is recommended in patients with a high PSA and/or very suspicious DRE results, if accessible. Since it is utilized with MRI/US fusion biopsy devices, mpMRI improves the CDR of csPCa significantly, and reduces CDR of lower-risk cancers.7,12-14 On the contrary, Thai guidelines still recommend 12-cores systematic TRUS biopsy as the gold standard in detection of PCa because of limited access to MRIs, scarcity of specialized radiologists, and a lack of other resources. However, this leads to a higher rate of false negatives and lower csPCa detection. When considering obvious beneficial evidence, Thai tertiary medical centers are starting to shift their focus towards targeted biopsies.

This study revealed an overall CDR of MRI/US fusion prostate biopsy was 12.99% higher compared to systemic biopsies, which had a detection rate of 45.72%. Our overall CDR was not different from other studies (47%-62.9%)4-7,12,15-17, but in our study, csPCa was higher than in studies of Kasivisvanathan et al.7, Ahdoot et al.12,

Choomark et al.



Benelli et al.5, and Hansen et al.6 Thus, this potentially illustrates how the MRI/US fusion prostate biopsy system at our institute is not inferior to other studies. Our identified predictors are similar to another study5 where PI-RADS is a strong predictor on the list in both overall PCa and csPCa, which advocates the use of an MRI before prostate biopsy, if possible. Moreover, this study confirmed that the higher PI-RADS, the greater the detection rate. After we studied the results of the univariate and multivariate analysis, we found that positive predictive factors for PCa detection were age, PSAD, and PI-RADS, whereas prostate volume was a negative predictive factor. Likewise the conclusion of Walton et al.17, CDR decreased with increasing prostate volume. Al-Khalil et al.18 suggested a larger prostate volume would lead to a lower positive CDR. It supposed that benign prostatic hyperplasia (BPH) caused transition zone (TZ) hyperplasia and led to atrophy and apoptosis of cell in peripheral zone (PZ), and this is the zone where most PCa develops. This decreases the likelihood of PCa in the remaining glands.

This study still recommends both systematic and targeted biopsies in MRI/US fusion prostate biopsy procedures because 34 (3.37%) out of 1,039 patients would be missed if targeted biopsy alone was done. Similar to the MRI-FIRST trial14, which studied naïve biopsy, our results showed that 5.2% of csPCa would be missed if both biopsies were skipped. As we experienced several cases that involved an unnecessary biopsy, which is a waste of both time and resources of our pathologists, we use the NNB method to estimate how many core tissues were needed to gain enough yield to detect cancer. Moreover, we hoped this method would further decrease the workload of pathologists. Several previous studies5,14 of biopsied targeted lesions revealed at least 3 cores per lesion, but they did not provide certain evidences for their recommendation. With our reporting system, which didn’t specify or detail histopathological information for each and every biopsied lesion for research purpose, the calculated NNB for multiple ROI would become too susceptible to bias to draw any trustworthy conclusion. Our study selected patients with single ROI and calculated NNB of targeted lesion in PI-RADS 3, 4, and 5. Since, these NNB was derived from patients with single ROI, interference on multiple ROI was limited. We hope this study inspires clinicians to develop a method to study NNB of multiple ROIs in the future.

This study had a few limitations. First, this study was a retrospective study at a single institution. Second, a version difference (v2.0 and v2.1) of PI-RADS existed in our cohort, so there may be some inconsistency in

distinguishing PI-RADS category 2 and 3, but PI-RADS 4 and 5 lesions are not affected. Third, the NNB we calculated was only usable for a single lesion.


CONCLUSION

This study supports the role of MRI/US fusion prostate biopsy in PCa detection. The combination of both targeted biopsy and systematic biopsy enhances CDR of PCa in comparison with systematic biopsy alone. The higher the PI-RADS on mpMRI was, the greater the csPCa detection rate. PI-RADS 3 mainly consisted of benign outcomes and ciPCa. Positive predictive factors for PCa detection were age, PSAD and PI-RADS, whereas prostate volume was a negative predictive factor. NNB is helpful in guiding the least amount of biopsied cores in single targeted lesion on MRI.


ACKNOWLEDGEMENTS

The author would like to express gratitude to Katunyou Mahamongkol, M.D., Miss Jitsiri Chaiyatho and the coordinators at Siriraj Hospital for their valuable contributions to this study.


Conflicts of interest

The authors declare they have no conflict of interest.


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