Faut-il réaliser des biopsies systématiques en cas d’IRM suspecte de cancer de prostate en 2020 ? Une revue de littérature

10 mars 2021

Auteurs : Q. Vesval, G. Fiard, A. Villers, J.M. Norris, J. Olivier
Référence : Prog Urol, 2021, 3, 31, 147-157




 




Introduction


Evidence suggests that multiparametric magnetic resonance imaging (mpMRI) before biopsy improves the detection of clinically significant prostate cancer (csPCa) with a high negative predictive value (NPV) of 85-95%, according to csPCa definition. Current guidelines recommend the use of mpMRI prior to biopsy in biopsy-naïve patients with a suspected prostate cancer (PCa). When a suspicious lesion is present, it is recommended to perform targeted biopsy (TB) and systematic biopsy (SB) [1]. In patients with prior negative biopsy and a persistent suspicion of PCa, saturation biopsies may be performed, increasing PCa detection, mainly represented by anterior lesions [2] with a potential for increased morbidity [3]. Similarly, when active surveillance (AS) is being proposed as an alternative to active treatment, it is not clear how biopsies should be performed as part of follow-up.


In the era of TB, precision medicine and focal therapy, the indications of SB are still under discussion. They are criticized as being responsible for the over-diagnosis of insignificant cancers. However, significant cancers can still be under-detected by imaging alone [4]. Can we estimate the added value of SB to TB?


In the case of a multi-focal cancer, mpMRI appears less effective in the detection of secondary or tertiary foci [5, 6]. When whole-gland treatment is planned, TB may be sufficient, and missing other foci may have no consequence besides a less adequate treatment planning and increased risk of surgical margin. However, what would be the consequences of omitting SB when considering focal therapy?


Finally, prostate biopsy is an invasive procedure, exposing the patient to a risk of morbidity, sometimes leading to severe complications and hospitalizations. To what extent does the multiplication of samples increase this morbidity?


We propose to answer these questions through a review of recent literature.


Methods


We performed a non-systematic review of the literature in April 2020, including the most recent articles (after 2015) in PubMed, using the following search terms: "MRI", "prostate cancer", "systematic biopsy", "targeted biopsy", "adverse events". All English titles and abstracts were reviewed and included if providing sufficient data to answer the study questions. References of the selected articles were screened for additional articles.


Results


Should we continue adding systematic to targeted cores?


It appears that no "one size fits all" answer can be provided to answer this question. Factors related to the patient (prostate volume, prior history of sepsis, prior history of biopsy), the targeting technique used (in-bore vs. cognitive vs. software fusion), the number of targeted cores obtained, the experience of the operator and the treatment planned (whole-gland vs. focal) all have to be taken into account. Still, review of the most recent literature can provide us with some answers by looking at the added value of systematic biopsies in patients undergoing both diagnostic modalities in various situations. Details are presented in Table 1.


Biopsy-naïve patients


Two prospective studies provide us with good quality evidence regarding biopsy-naïve men. In the MRI-first trial, 251 biopsy-naïve patients received a combination of 12 systematic and three targeted biopsies (with cognitive or software guidance). Adding systematic cores led to the diagnosis of 13 (+5.2%) supplementary significant cancers [7]. In the 4M study, 317 patients were enrolled who underwent 2-4 in-bore targeted biopsies and systematic (12 cores) sampling. The added value of the latter was +7% [8]. Similarly, an added value of +6% was found in a retrospective analysis of 214 patients evaluated by a mean of 6 (range 2-15) targeted biopsies and 12 systematic cores (range 6-18) [9].


Prior negative biopsy


Although previously published studies showed a tendency toward an increased added value of SB among patients with a previous history of negative biopsy from 6.4% to 12.6% [10, 11], other recent studies are in contradiction with these results, where added values were between 1.7% and 3.5% [12, 13]. In the most recent prospective study (FUTURE trial), among 152 patients having both SB and TB, the detection rate for csPCa was 35% (34% by TB and 16% by SB) and the added value of SB was only 1.3% [14].


A Cochrane review and meta-analysis determined an estimated added-value around +5% for biopsy-naïve patients and around +2.5% for patients with previous negative biopsies, with a significant uncertainty in both situations but especially for biopsy-naïve patients [15].


Active surveillance


In the ASIST trial, 273 patients on AS for PCa were randomized between SB alone and mpMRI with systematic and targeted biopsies (MRI arm) for confirmatory biopsy. No difference was observed in the detection rate of csPCa (27% of patients in the SB arm and 33% in the MRI arm). In the MRI arm, upgrading was seen in 15% of patients and the added value of SB was 7.9% [16]. On confirmatory biopsy, overall upgrading to cancer grade group ≥2 was 26-33% and the added value of repeat SB in MRI-positive men was 36-48% [10, 17, 18] at one-year follow-up of low-risk PCa. A lower overall upgrading rate (14-16%) at confirmatory biopsy and lower added value of repeat SB in MRI-positive men (12-18%) were reported by Thurtle et al. [19] and Elkjaer et al. [20], which could be explained by a cohort of very-low-risk PCa men. In a recent retrospective study, on 101 men on AS who had follow-up MRI and SB+TB, the added value of SB was 17% [21].


Mixed population


In a very recent study including 2103 patients with a suspicious mpMRI, including biopsy-naïve, prior negative biopsy and active surveillance patients, Ahdoot et al. demonstrated an added value of 12 systematic cores around +5.8%, for the detection of clinically significant cancer [22]. Similarly, a prospective study enrolling 255 patients subjected to 2-4 targeted cores and 12 systematic cores reported an added value of 5% [11]. Furthermore, comparable results were obtained in two retrospective studies including 191 and 116 patients, with an added value of 12 systematic cores estimated at +6.8% and +6.9%, respectively [23, 24]. Conversely, Oderda and colleagues determined an added value of +9% in a retrospective multicentre study including 2115 patients. However, this was probably explained by the high added value of systematic biopsies in the subgroup of patients under active surveillance in this study (+33%) [10]. Neale et al. have shown a +12% added value of SB on 282 patients, a higher value due to a higher proportion of biopsy-naïve patients. In this cohort, TB in patients with Likert score 3 lesion detect only 73% of csPCa, the other 27% were picked by SB, while TB in patients with Likert score 5 lesion allow detection of 100% of csPCa. As an alternative of both SB+TB, an "extended targeted" biopsy method, with four TB and six same-quadrant-only SB, allows detection of 97% csPCa but authors also concluded that contralateral SB allow better treatment planification, notably in a nerve sparing approach [25].


Correlation in Gleason Grade Group (GGG) between biopsy and radical prostatectomy specimen


Calio et al. showed that in a cohort of 208 patients, the proportion of patients who experienced upgrading of GGG at radical prostatectomy was 47.1%, 30.1% and 18.8% respectively, according to SB only, TB only and combined SB+TB [26]. Moreover, Diamand et al. evaluated the accuracy in GGG by comparing histopathology between SB, TB and SB+TB and RP among 443 patients in a retrospective study. Concordance was 49.4%, 51.2% and 63.2%, respectively, for overall PCa. Combining both techniques (SB+TB) achieves a 56.7% in concordance with final pathology, an upgrade of 30% and a downgrade of 13.3% for csPCa, with significant difference in comparison with the two biopsy techniques separately [27]. More recently, Gandaglia et al. have shown that SB+TB reduces the rate of upgrading at RP to 27% (versus 32% with TB alone) [28]. Same results were observed by Ahdoot et al., where rates of any upgrading or cancer significant upgrading on whole mount was higher for SB (41.6% vs. 16.8%) and TB (30.9% and 8.7%) than for combined biopsy (14.4% and 3.5%), with low rates of downgrading to GGG 1 (2.2%, 2.5% and 3.7% respectively) [22].


Are systematic biopsies still necessary in the era of partial gland ablation?


Partial gland ablation (PGA) has emerged as a treatment option for men with clinically localized PCa. It is defined as an "individualized treatment that selectively ablates known disease and preserves existing function, with the overall objective of minimizing morbidity without compromising life expectancy" [29]. The principal pitfall of PGA lies in the multifocality of PCa. Histological studies have shown in men undergoing radical prostatectomy that approximatively 42% harbor unifocal tumors and only 21% have unilateral disease [30].


As PCa is multifocal in the majority of cases, treatment of the index lesion and surveillance of clinically insignificant foci has been proposed.


The precise identification of the volume, grade and location of all significant tumors within the prostate is key to the selection of patients before PGA. Besides, mpMRI also provides information on anatomical features required for patient selection, treatment planning and the choice of focal treatment energy. Patients are currently selected based on the results of TB, SB and their concordance with the mpMRI, although the sole treatment of MRI-visible tumors is being increasingly considered. Are SB still necessary in the era of mpMRI and focal treatments?


The ideal study design to answer our question would include a longitudinal follow-up of patients treated by PGA after an evaluation consisting in MRI and TB alone, to evaluate the clinical consequence of the omission of SB. However, such studies are not available in the current literature.


To answer this question with extant evidence, it is important to distinguish the diagnostic performances of mpMRI at a prostate level versus at a lesion level. Indeed, the excellent NPV of mpMRI demonstrated at the prostate level around 85% to 95% for csPCa does not seem to hold when analyzing at a lesion level [7]. Whole-mount pathology is the not ideal reference standard for correlating individual prostate lesions to mpMRI findings in the context of PGA because it does not take into account the potential follow-up of untreated lesions, but it can help define the added value of SB offering whole-gland sampling. Nassiri et al. have shown in 175 men, eligible for focal therapy based on TB, and treated by radical prostatectomy, that mpMRI and TB alone offered a sensitivity of 73.3%, and a specificity of 47.9%, with an accuracy of 54.7% [5]. Johnson et al. showed on 1213 pathologically confirmed tumor foci in 588 patients that mpMRI missed 55% of all lesions, including 35% of csPCa and approximatively 20% of high-grade PCa. Even though the majority of undetected multifocal tumors were clinically insignificant, 31% of the 629 undetected foci contained Gleason pattern 4 at final pathology. The low sensitivity at lesion level, and the proportion of men with undetected significant tumor foci are limitations of using mpMRI and TB alone when considering PGA treatment [6].


However, none of these studies looked at the proportion of patients with bilateral disease, including contralateral clinically insignificant tumor. Karavitakis et al. showed on 100 consecutive radical prostatectomy specimens that Gleason score and pathological stage were almost invariably defined by the index lesion. Satellite lesions tended to be small and well differentiated. However, these results should be interpreted with caution because no preoperative data were included and no absolute conclusions can be done from their analysis about the biological consequence of tumor focality due to the absence of follow-up data [31]. Furthermore, the presence of clinically insignificant cancer in the non-treated area had no influence on the radical treatment-free survival, nor on clinically significant cancer-free survival on a retrospective study on 55 patients [32].


Based on these results, it seems reasonable to recommend combining systematic biopsy with mpMRI-TB to improve patient selection and confirm eligibility to focal therapy. This was reinforced by a Delphi consensus on the use of mpMRI for the detection of PCa in focal therapy, stating that additional systematic biopsy remains crucial for accurate evaluation and patient selection [33].


Is there an increased morbidity when adding SB to TB?


The use of TB alone may decrease biopsy-related complications, but the clinical relevance of this remains unproven. While the impact of the transperineal versus transrectal route on adverse events (AEs) is still controversial, the assessment of the impact of the number of biopsy cores on AEs could help provide answers to this question. Few comparative studies have provided detailed complication rates (Table 2). Prostate biopsies are associated with a relatively frequent rate of bleeding events such as hematuria, hematochezia, haematospermia, reported with a high incidence variability (respectively 2-84%, 1.3-45% and 1.1-92.6%), but these AEs tend to be mild, self-limiting and transient [34]. Furthermore, there is no obvious correlation between the risk of bleeding and the number of biopsy cores taken. According to Eineluoto et al. [35], patients undergoing three-cores TB experienced less haematuria and pain compared with those undergoing 12-cores SB; however, the results regarding other bleeding events were not significant. Similarly, in the FUTURE trial, the in-bore MRI-TB group (with fewer biopsy cores taken) reported less episodes of haematuria and haematospermia, and anticoagulant usage was not associated with increased risk of bleeding complication [36].


A short term exacerbation of low urinary tract symptoms (LUTS) is another common side effect after PB with reported rates ranging from 6 to 25%, which may lead to acute urinary retention (AUR) [34]. In addition to the number of biopsy cores, the route used for biopsies and the transitional zone volume appeared associated to the occurrence of AUR. AUR was more frequent with the transperineal (1.7-11.1%) than transrectal approach (4.2% vs. 0.9%) [37]. In biopsy-naïve patients, Murray et al. showed that the International Prostate Symptom Score (IPSS) was significantly increased at one week and four weeks after biopsy, but returned to baseline after three months [38]. In contrast, Wegelin et al. did not find any significant impact on self-reported LUTS at 30-days post biopsy [36]. According to Fujita et al., there was no significantly difference in IPSS regardless of the number of PBs performed in men on AS [39].


Erectile dysfunction may (ED) occur in a significant number of men undergoing PBs; however it appeared to be mild and transient, with complete recovery after one to six months [34]. As ED could be multifactorial, with physical and psychological aspects both involved (anxiety regarding the possibility of cancer, haematospermia and its detrimental effect on sexual activity), a relationship with the number of biopsy cores still has to be demonstrated. In 2016, Murray et al. described decreased IIEF5 score (International Index of Erectile Function) in biopsy-naïve patients at 1 week, 4 weeks and 3 months [38]. In contrast, in patients with a history of prior negative biopsy, no significant impact on self-reported ED at 30 days after biopsy was noted [36]. In men on AS, increasing the number of biopsies was associated with a decrease in Sexual Health Inventory for Men score (SHIM). A past history of 3 or more biopsy series was associated with a greater decrease in SHIM compared to 2 or fewer biopsy series [39]. Klein et al. concluded that ED was transiently affected by prostate biopsy regardless of the number of cores [40].


The rate of clinical infectious complications ranges approximately from 1-17.5%. Fluoroquinolone-Resistant Escherichia Coli is the most recognized risk factor, independently of medical comorbidities (particularly diabetes and metabolic syndrome) and older age [34]. Transrectal biopsy was associated with a higher burden of sepsis than transperineal (0.8% vs. 0.1%) [37]. According to Pilatz et al., increasing the number of biopsy cores did not result in increased infectious complications [41]. However, repeating biopsy series did appear to increase the risk of infection, up to a rate of 15% for patient with five or more previous biopsy series [42]. Each additional biopsy session was associated with a 1.7-fold increase in overall hospitalizations and 1.7-fold increase in serious infectious complications [43]. Conversely, the low incidence of hospitalization and infectious complications after in-bore transperineal MRI-targeted biopsy appears related to the biopsy route rather than the number of cores taken [44].


In the PRECISION trial, complications in biopsy-naïve patients reported at 30 days were less frequent in the mpMRI-TB group than in the SB group, but fewer biopsy cores were obtained in the former group; serious AEs, represented by prostatitis, sepsis and hematuria, were observed in 2% in both groups [45]. In the FUTURE trial, SB increased the risk of AEs with an odd-ratio of 1.1 per additional core taken [36].


The hospitalization rate within 30 days post biopsy for AEs ranged between 1.4-6.9%, mainly represented by infection, with age and comorbidity as independent predictor factor, and showed a steady increase over time [46]. Mortality after PB remains uncommon; to date, most PB-related deaths are due to septicemia and septic shock. Repeat biopsy does not appear to be associated with a higher overall mortality rate [43].


Discussion


The performance of mpMRI has now become key for the detection and treatment decision-making for patients suspected of having PCa. It is now endorsed by most guidelines before prostate biopsy, allowing the addition of TB. However, since its NPV is not 100%, there is a risk of non-detecting significant lesions, especially since PCa is usually a multifocal disease.


All three issues considered in this review rely on the risk-benefit balance of the performance of prostate biopsies. The added value of SB to TB in the most recently published studies ranged from 5 to 7% with a remarkable consistency between studies for the detection of significant cancers, defined by cancers greater than or equal to GGG 2. This added value appears significant for biopsy-naïve patients, among whom a precise characterization of lesions is essential for treatment planning and stratification and allow for the detection of lesions that are not visible on mpMRI. Using SB and TB simultaneously provide less upgrading and better concordance with final pathological report on prostatectomy specimen. This is of particular importance when focal therapy is considered, while whole-gland treatment would alleviate the risk of neglecting a significant lesion outside the treated field. Gandaglia et al. are also suggesting adding concomitant SB leads to better risk stratification, with better concordance and less upgrading between GGG on biopsy and on radical prostatectomy specimen. Moreover, presence of csPCa at concomitant SB to TB was associated with an increased risk of extra-capsular extension and seminal vesicle invasion on RP specimen [28], and percentage of positive cores on SB is a significant predictor for positive margin during nerve sparing robot-assisted RP [47], confirming the value of SB implementation for treatment planning.


Conversely, in patients with a previous history of negative SB, the remaining significant lesions are more often found in the anterior part of the gland and likely to be missed by subsequent SB. Saturation biopsies, as performed before the emergence of mpMRI, are less likely to have a significant added-value and are associated with greater morbidity, as showed in the PICTURE study, where AUR occurs in 24% of patients, with a median of 49 cores taken with a transperineal approach. In the FUTURE study, the added value of SB after a prior negative biopsy series appeared limited as the performance of these biopsies would detect only 1.3% additional significant cancers [14].


For patients on active surveillance, the performance of follow-up biopsies is recommended, but the replacement of this invasive procedure by an imaging-based surveillance, and biopsies triggered only in case of mpMRI changes, is being increasingly adopted. A recent review of the literature [48] reported 13 cohorts of patients under active surveillance, using many AS protocols. All authors agreed that repeated PSA measurements were important, and most authors recommended the performance of confirmatory biopsies within 12 months and up to 2 years after the initial diagnosis if mpMRI was not performed at inclusion. The latest EAU guidelines now support the absence of confirmatory biopsies provided the patient had an upfront mpMRI with TB and SB [49]. Patients under AS with positive MRI have higher risk of csPCa, explaining high added value of SB in these patients, especially since mpMRI could miss multifocal disease. Therefore, follow-up biopsies should include both TB and SB, as upgrading is key for the continuation of AS, and SB has been shown to add significant value in this regard [17, 18, 19, 20]. In the ASIST trial, the addition of mpMRI with TB to SB initially did not significantly increase the upgrading rate compared with SB alone at time of confirmatory biopsy and the addition of 2-cores TB led to a non-statistically significant reduced upgrading than SB with 12 cores (14% vs. 23% respectively) [16]. However, the 2-year biopsy results recently published demonstrated a higher rate of progression in SB arm only vs. MRI-arm (13% vs. 27%, P =0.021) [50]. Conversely, Chesnut et al. concluded that performing biopsy only in clinical or mpMRI changes at 3 years in patients on AS could avoid many biopsies (estimated at 681 per 1000 men) but miss an unacceptable amount (16.9%) of clinically significant diseases [21].


The expertise of the centers should be taken into consideration since there may be major differences on the precision of TB, especially when performed under cognitive guidance [50]. All the studies included in this review were performed in expert centers, with trained physicians. In patients considered at higher risk of occult higher-grade disease, SB should be performed regardless of the mpMRI findings, and an increased sampling density should probably be offered.


Besides these considerations, the decision to biopsy and the biopsy technique used should also be based on the patients individualized risk of complications. All invasive procedures carry risk, and the tolerance for this risk depends on the potential benefits of the intervention and needs to be based on a shared decision-making approach. Post-biopsy infectious complications have been linked to older patient age and medical comorbidity status, emphasizing the importance of careful selection before biopsy. The transperineal approach appears to be safer regarding infectious complications, probably because of the avoidance of transrectal bacteria contamination. Similarly, the low incidence of infection after MRI-guided in-bore biopsy possibly resulted from the lower number of cores taken with this approach. Many patients experienced transient LUTS, and only a small proportion of these patients experienced urinary retention. Biopsy repletion, as opposed to number of biopsy cores taken, appears to drive the infectious morbidity in a cumulative fashion. A better upfront staging with pre-biopsy mpMRI and TB, and the implementation of mpMRI in AS protocols should help mitigate this risk. However, transperineal and limited sampling with MRI targeted biopsy appears to be associated with a reduced risk of severe infectious complications, and although not available for all patients, these approaches should certainly be considered for patients at higher risk of sepsis.


Conclusion


In the presence of a suspicious mpMRI lesion, SB added to TB appear to have a moderate added value in biopsy-naïve patients, and a significant added value in patients under AS. However, SB can likely be omitted in patients with a history of prior negative biopsies, due to minimal additional benefit in this sub-group. If focal treatment is considered, SB appears to be necessary to aid with optimal surgical planning. Severe complications from biopsies do not appear to increase with the number of cores, but rather with the number of previous biopsy series.


Disclosure of interest


The authors declare that they have no competing interest.



Acknowledgments


Gaelle Fiard receives funding from and wishes to thank the Fondation de France and the European Urology Scholarship Program. Joseph Norris receives funding from the Medical Research Council (UK).




Table 1 - Added value of systematic biopsies in addition to targeted biopsies.
Reference  Inclusion period  Design  MRI type  Patients having MRI+TBx+SBx (n TBx type  TBx cores (n SBx cores (n Clinically-significant cancers on TBx n (%)  Clinically-significant cancers on SBx n (%)  Clinically-significant cancers total n (%)  Definition clinically-significant cancer a,b, tblfn0010  Added value SBx 
Biopsy-naïve patients 
Rouvière 2018 (MRI first) [7 2015-2016  Prospective  1.5T or 3 251  Cognitive/Fusion  12  81 (32.2)  75 (29.9 %)  94 (37 %)  GGG ≥ +5.2 % 
Van der Leest 2019 (4M) [8 2015-2017  Prospective  3 317  In-bore  2-4  12  159 (50 %)  146 (46 %)  180 (57 %)  GGG ≥ +7 % 
Borkowetz 2018 [9 2015-2017  Retrospective  3 214  Fusion  12  81 (38 %)  74 (35 %)  94 (44 %)  GGG ≥ +6 % 
Prior negative biopsy 
Exterkate 2020 [14 2014-2017  Prospective  3 152  Fusion/Cognitive  >2  10-12  51 (33.6 %)  24 (15.8 %)  53 (34.9 %)  GGG ≥ +1.3 % 
Mendhiratta 2015 [13 2012-2014  Retrospective  3 172  Fusion  3-4  12  28 (16.3 %)  16 (9.3 %)  31 (18 %)  GGG ≥ +1.7 % 
Salami 2015 [12 2012-2014  Prospective  3 140  Fusion  12  67 (47.9 %)  43 (30.7 %)  72 (51.4 %)  GGG ≥ +3.5 % 
Active surveillance 
Confirmatory biopsy                         
Klotz 2019 (ASIST) [16 2011-2015  Prospective  3 127  Fusion  2-3  12  19 (14.9 %)  21 (16.5 %)  29 (22.8 %)  GGG ≥ +7.9 % 
Osses 2020 [18 2013-2019  Retrospective  1.5T or 3 111  Fusion  2-5  10-12  20 (18 %)  28 (25 %)  35 (32 %)  GGG ≥ +14 % 
Hamoen 2018 [17 2009-2013  Prospective  3 75  In-Bore  2-4  10  9 (12 %)  15 (20 %)  33 (44 %)  GGG ≥ +8 % 
Repeat biospy                         
Chesnut 2020 [21 2013-2016  Retrospective  3 101  Fusion  2-3  14  22 (21.7 %)  35 (34.7 %)  39 (38.6 %)  GGG ≥ +16.9 % 
Mixed population 
Ahdoot 2020 [22 2007-2019  Retrospective  3 2103  Fusion  12  795 (38%)  650 (31%)  918 (44%)  GGG ≥ +5.8% 
        Biopsy-naïve
Prior negative biopsy
Prior positive biopsy 
436
873
794 
    NA
NA
NA 
NA
NA
NA 
NA
NA
NA 
  NA
NA
NA 
Mannaerts 2019 [11 2015-2018  Prospective  1.5T or 3 255  Fusion  2-4  12  113 (44%)  110 (43%)  126 (49%)  GGG ≥ +5% 
        Biopsy-naïve
Prior negative biopsy 
161
94 
    94 (58%)
19 (20%) 
92 (57%)
18 (19%) 
101 (63%)
25 (27%) 
  +4.3%
+6.4% 
Fourcade 2018 [23 2013-2016  Retrospective  3 191  Fusion  2-4  10-12  73 (38%)  64 (33.5%)  86 (45%)  GGG ≥2+  +6.8% 
        Biopsy-naïve
Prior negative biopsy 
95
96 
    NA
NA 
NA
NA 
NA
NA 
  NA
NA 
Freifeld 2019 [24 2016-2017  Retrospective  3 116  Fusion  2-3  12  47 (40.5%)  NA  55 (47%)  GGG ≥ +6.9% 
        Biopsy-naïve
Prior negative biopsy
Prior positive biopsy 
55
43
18 
    NA
NA
NA 
NA
NA
NA 
NA
NA
NA 
  NA
NA
NA 
Oderda 2018 [10 2010-2017  Retrospective  1.5T or 3 2115  Fusion  10  716 (34%)    909 (43%)  GGG ≥ +9% 
        Biopsy-naïve
Prior negative biopsy
Prior positive biopsy 
705
741
63 
    371 (53%)
299 (40%)
31 (49%) 
NA
NA
NA 
420 (59.6%)
393 (53%)
52 (82%) 
  +6.9%
+12.6%
+33% 



Légende :
TBx=targeted biopsies; SBx=systematic biopsies; NA=not available.

[a] 
When several definitions are used in the study, we present here the results for GGG ≥ 2.
[b] 
GGG ≥ 2+ means a broader definition is used.


Table 2 - Comparison of AEs occurrence.
Authors  Technique  Patients  TB Cores  SB Cores  Adverse Event reported at 30-d evaluation 
      n (IQR)  n (IQR)  Pain  Hematuria  Hemato-spermia  Rectal bleeding  Fever  UTI  AUR  ED 
Eineluoto 2018 [35 TB (Fusion)  59  3 (3-5)  12 (20%) a  26 (44%) a  23 (39%)  11 (19%)  1 (2%)  N/A  N/A  N/A 
  SB  203  12 (all)  70 (34%) a  140 (69%) a  94 (46%)  65 (32%)  11 (5%)  N/A  N/A  N/A 
Wegelin 2019 [36 TB+SB (cog. TR)  78  3 (3-4)  10 (8-12)  N/A  58 (74%) a  39 (50%) a  4 (5.1%)  4 (5.1%)  6.4 (5%)  4 (5.1%)  N/A 
  TB+SB (Fusion TP)  79  4 (3-5)  10 (8-12)  N/A  40 (51%) a  28 (35%) a  2 (2.5%)  2 (2.5%)  1 (1.3%)  3 (3.8%)  N/A 
  TB (in-bore TR)  77  2 (2-3)  N/A  27 (36%) a  20 (26%) a  2 (2.6%)  1 (1.3%)  2 (2.6%)  0 (0%)  N/A 
Kasivisvanathan 2018 [45 MRI-TB  252  4 (3-7)  27 (13%)  64 (30%)  68 (32%)  30 (14%)  9 (4.2%)  5 (2.4%)  3 (1.4%)  23 (11%) 
  SB  248  10-12  48 (23%)  129 (63%)  123 (60%)  45 (22%)  9 (4.4%)  2 (1%)  2 (1%)  32 (16%) 



Légende :
TB=targeted biopsy; SB=Systematic biopsy; IQR=interquartile range; COG: cognitive fusion transrectal biopsy; TR=transrectal; TP=transperineal.

[a] 
Significative result.


References



Rozet F., Hennequin C., Beauval J.-B., Beuzeboc P., Cormier L., Fromont-Hankard G., et al. Recommandations françaises du Comité de Cancérologie de l'AFU-Actualisation 2018-2020: cancer de la prostate Prog En Urol 2018 ;  28 (12) : S79-S130 [inter-ref]
Ong W.L., Weerakoon M., Huang S., Paul E., Lawrentschuk N., Frydenberg M., et al. Transperineal biopsy prostate cancer detection in first biopsy and repeat biopsy after negative transrectal ultrasound-guided biopsy: the Victorian Transperineal Biopsy Collaboration experience BJU Int 2015 ;  116 (4) : 568-576 [cross-ref]
Miah S., Eldred-Evans D., Simmons L.A.M., Shah T.T., Kanthabalan A., Arya M., et al. Patient Reported Outcome Measures for Transperineal Template Prostate Mapping Biopsies in the PICTURE Study J Urol 2018 ;  200 (6) : 1235-1240 [cross-ref]
Norris J.M., Carmona Echeverria L.M., Bott S.R.J., Brown L.C., Burns-Cox N., Dudderidge T., et al. What Type of Prostate Cancer Is Systematically Overlooked by Multiparametric Magnetic Resonance Imaging? An Analysis from the PROMIS Cohort Eur Urol 2020 ; [S030228382030261X].
Nassiri N., Chang E., Lieu P., Priester A.M., Margolis D.J.A., Huang J., et al. Focal Therapy Eligibility Determined by Magnetic Resonance Imaging/Ultrasound Fusion Biopsy J Urol 2018 ;  199 (2) : 453-458 [cross-ref]
Johnson D.C., Raman S.S., Mirak S.A., Kwan L., Bajgiran A.M., Hsu W., et al. Detection of Individual Prostate Cancer Foci via Multiparametric Magnetic Resonance Imaging Eur Urol 2019 ;  75 (5) : 712-720 [cross-ref]
Rouvière O., Puech P., Renard-Penna R., Claudon M., Roy C., Mège-Lechevallier F., et al. Use of prostate systematic and targeted biopsy on the basis of multiparametric MRI in biopsy-naive patients (MRI-FIRST): a prospective, multicentre, paired diagnostic study Lancet Oncol 2019 ;  20 (1) : 100-109 [inter-ref]
van der Leest M., Cornel E., Israël B., Hendriks R., Padhani A.R., Hoogenboom M., et al. Head-to-head Comparison of Transrectal Ultrasound-guided Prostate Biopsy Versus Multiparametric Prostate Resonance Imaging with Subsequent Magnetic Resonance-guided Biopsy in Biopsy-naïve Men with Elevated Prostate-specific Antigen: A Large Prospective Multicenter Clinical Study Eur Urol 2019 ;  75 (4) : 570-578 [cross-ref]
Borkowetz A., Hadaschik B., Platzek I., Toma M., Torsev G., Renner T., et al. Prospective comparison of transperineal magnetic resonance imaging/ultrasonography fusion biopsy and transrectal systematic biopsy in biopsy-naïve patients BJU Int 2018 ;  121 (1) : 53-60 [cross-ref]
Oderda M., Marra G., Albisinni S., Altobelli E., Baco E., Beatrici V., et al. Accuracy of elastic fusion biopsy in daily practice: Results of a multicenter study of 2115 patients Int J Urol 2018 ;  25 (12) : 990-997 [cross-ref]
Mannaerts C.K., Kajtazovic A., Lodeizen O.A.P., Gayet M., Engelbrecht M.R.W., Jager G.J., et al. The added value of systematic biopsy in men with suspicion of prostate cancer undergoing multiparametric MRI-targeted biopsy Urol Oncol Semin Orig Investig 2019 ;  37 (5) : [298.e1-298.e9].
Salami S.S., Ben-Levi E., Yaskiv O., Ryniker L., Turkbey B., Kavoussi L.R., et al. In patients with a previous negative prostate biopsy and a suspicious lesion on magnetic resonance imaging, is a 12-core biopsy still necessary in addition to a targeted biopsy?.: Performance of mpMRI in predicting prostate cancer on repeat biopsy BJU Int 2015 ;  115 (4) : 562-570 [cross-ref]
Mendhiratta N., Meng X., Rosenkrantz A.B., Wysock J.S., Fenstermaker M., Huang R., et al. Prebiopsy MRI and MRI-ultrasound Fusion-targeted Prostate Biopsy in Men With Previous Negative Biopsies: Impact on Repeat Biopsy Strategies Urology 2015 ;  86 (6) : 1192-1199 [inter-ref]
Exterkate L., Wegelin O., Barentsz J.O., van der Leest M.G., Kummer J.A., Vreuls W., et al. Is There Still a Need for Repeated Systematic Biopsies in Patients with Previous Negative Biopsies in the Era of Magnetic Resonance Imaging-targeted Biopsies of the Prostate? Eur Urol Oncol 2020 ;  3 (2) : 216-223 [cross-ref]
Drost F-JH, Osses D.F., Nieboer D., Steyerberg E.W., Bangma C.H., Roobol M.J., et al. Prostate MRI, with or without MRI-targeted biopsy, and systematic biopsy for detecting prostate cancer. Cochrane Urology Group, éditeur Cochrane Database Syst Rev [Internet] 2019 ; 10.1002/14651858.CD012663.pub2[cité 25 avr 2020].
Klotz L., Loblaw A., Sugar L., Moussa M., Berman D.M., Van der Kwast T., et al. Active Surveillance Magnetic Resonance Imaging Study (ASIST): Results of a Randomized Multicenter Prospective Trial Eur Urol 2019 ;  75 (2) : 300-309 [cross-ref]
Hamoen E.H.J., Hoeks C.M.A., Somford D.M., van Oort I.M., Vergunst H., Oddens J.R., et al. Value of Serial Multiparametric Magnetic Resonance Imaging and Magnetic Resonance Imaging-guided Biopsies in Men with Low-risk Prostate Cancer on Active Surveillance After 1 Yr Follow-up Eur Urol Focus 2019 ;  5 (3) : 407-415 [cross-ref]
Osses D.F., Drost F-JH, Verbeek J.F.M., Luiting H.B., van Leenders G.J.L.H., Bangma C.H., et al. Prostate cancer upgrading with serial prostate MRI scans and repeat biopsy in men on active surveillance: are confirmatory biopsies still necessary? BJU Int [Internet] 2020 ; 10.1111/bju.15065
Thurtle D., Barrett T., Thankappan-Nair V., Koo B., Warren A., Kastner C., et al. Progression and treatment rates using an active surveillance protocol incorporating image-guided baseline biopsies and multiparametric magnetic resonance imaging monitoring for men with favourable-risk prostate cancer BJU Int 2018 ;  122 (1) : 59-65 [cross-ref]
Elkjær M.C., Andersen M.H., Høyer S., Pedersen B.G., Borre M. Multi-parametric magnetic resonance imaging monitoring patients in active surveillance for prostate cancer: a prospective cohort study Scand J Urol 2018 ;  52 (1) : 8-13
Chesnut G.T., Vertosick E.A., Benfante N., Sjoberg D.D., Fainberg J., Lee T., et al. Role of Changes in Magnetic Resonance Imaging or Clinical Stage in Evaluation of Disease Progression for Men with Prostate Cancer on Active Surveillance Eur Urol 2020 ;  77 (4) : 501-507 [cross-ref]
Ahdoot M., Wilbur A.R., Reese S.E., Lebastchi A.H., Mehralivand S., Gomella P.T., et al. MRI-Targeted Systematic, and Combined Biopsy for Prostate Cancer Diagnosis N Engl J Med 2020 ;  382 (10) : 917-928 [cross-ref]
Fourcade A., Payrard C., Tissot V., Perrouin-Verbe M.-A., Demany N., Serey-Effeil S., et al. The combination of targeted and systematic prostate biopsies is the best protocol for the detection of clinically significant prostate cancer Scand J Urol 2018 ;  52 (3) : 174-179 [cross-ref]
Freifeld Y., Xi Y., Passoni N., Woldu S., Hornberger B., Goldberg K., et al. Optimal sampling scheme in men with abnormal multiparametric MRI undergoing MRI-TRUS fusion prostate biopsy Urol Oncol Semin Orig Investig 2019 ;  37 (1) : 57-62 [cross-ref]
Neale A., Stroman L., Kum F., Jabarkhyl D., Di Benedetto A., Mehan N., et al. Targeted and systematic cognitive freehand-guided transperineal biopsy: is there still a role for systematic biopsy? Freehand TP Bx: is target alone enough? BJU Int 2020 ;  126 (2) : 280-285 [cross-ref]
Calio B.P., Sidana A., Sugano D., Gaur S., Maruf M., Jain A.L., et al. Risk of Upgrading from Prostate Biopsy to Radical Prostatectomy Pathology-Does Saturation Biopsy of Index Lesion during Multiparametric Magnetic Resonance Imaging-Transrectal Ultrasound Fusion Biopsy Help? J Urol 2018 ;  199 (4) : 976-982 [cross-ref]
Diamand R., Oderda M., Al Hajj Obeid W., Albisinni S., Van Velthoven R., Fasolis G., et al. A multicentric study on accurate grading of prostate cancer with systematic and MRI/US fusion targeted biopsies: comparison with final histopathology after radical prostatectomy World J Urol 2019 ;  37 (10) : 2109-2117 [cross-ref]
Gandaglia G., Ploussard G., Valerio M., Mattei A., Fiori C., Roumiguié M., et al. The Key Combined Value of Multiparametric Magnetic Resonance Imaging, and Magnetic Resonance Imaging-targeted and Concomitant Systematic Biopsies for the Prediction of Adverse Pathological Features in Prostate Cancer Patients Undergoing Radical Prostatectomy Eur Urol 2020 ;  77 (6) : 733-741 [cross-ref]
Bostwick D.G., Waters D.J., Farley E.R., Meiers I., Rukstalis D., Cavanaugh W.A., et al. Group Consensus Reports from the Consensus Conference on Focal Treatment of Prostatic Carcinoma, Celebration, Florida, February 24, 2006 Urology 2007 ;  70 (6) : S42-S44 [inter-ref]
Nevoux P., Ouzzane A., Ahmed H.U., Emberton M., Montironi R., Presti J.C., et al. Quantitative tissue analyses of prostate cancer foci in an unselected cystoprostatectomy series: Prostate cancer foci in an unselected cystoprostatectomy series BJU Int 2012 ;  110 (4) : 517-523 [cross-ref]
Karavitakis M., Winkler M., Abel P., Livni N., Beckley I., Ahmed H.U. Histological characteristics of the index lesion in whole-mount radical prostatectomy specimens: implications for focal therapy Prostate Cancer Prostatic Dis 2011 ;  14 (1) : 46-52 [cross-ref]
Annoot A., Olivier J., Valtille P., Deken V., Leroy X., Puech P., et al. Extra-target low-risk prostate cancer: implications for focal high-intensity focused ultrasound of clinically significant prostate cancer World J Urol 2019 ;  37 (2) : 261-268 [cross-ref]
Tay K.J., Scheltema M.J., Ahmed H.U., Barret E., Coleman J.A., Dominguez-Escrig J., et al. Patient selection for prostate focal therapy in the era of active surveillance: an International Delphi Consensus Project Prostate Cancer Prostatic Dis 2017 ;  20 (3) : 294-299 [cross-ref]
Borghesi M., Ahmed H., Nam R., Schaeffer E., Schiavina R., Taneja S., et al. Complications After Systematic, Random, and Image-guided Prostate Biopsy Eur Urol 2017 ;  71 (3) : 353-365 [cross-ref]
Eineluoto J.T., Järvinen P., Kilpeläinen T., Lahdensuo K., Kalalahti I., Sandeman K., et al. Patient Experience of Systematic Versus Fusion Prostate Biopsies Eur Urol Oncol 2018 ;  1 (3) : 202-207 [cross-ref]
Wegelin O., Exterkate L., van der Leest M., Kelder J.C., Bosch J.L.H.R., Barentsz J.O., et al. Complications and Adverse Events of Three Magnetic Resonance Imaging-based Target Biopsy Techniques in the Diagnosis of Prostate Cancer Among Men with Prior Negative Biopsies: Results from the FUTURE Trial, a Multicentre Randomised Controlled Trial Eur Urol Oncol 2019 ;  2 (6) : 617-624 [cross-ref]
Bennett H.Y., Roberts M.J., Doi S.A.R., Gardiner R.A. The global burden of major infectious complications following prostate biopsy Epidemiol Infect 2016 ;  144 (8) : 1784-1791 [cross-ref]
Murray K.S., Bailey J., Zuk K., Lopez-Corona E., Thrasher J.B. A prospective study of erectile function after transrectal ultrasonography-guided prostate biopsy BJU Int 2015 ;  116 (2) : 190-195 [cross-ref]
Fujita K., Landis P., McNeil B.K., Pavlovich C.P. Serial Prostate Biopsies are Associated With an Increased Risk of Erectile Dysfunction in Men With Prostate Cancer on Active Surveillance J Urol 2009 ;  182 (6) : 2664-2669 [cross-ref]
Klein T., Palisaar R.J., Holz A., Brock M., Noldus J., Hinkel A. The Impact of Prostate Biopsy and Periprostatic Nerve Block on Erectile and Voiding Function: A Prospective Study J Urol 2010 ;  184 (4) : 1447-1452 [cross-ref]
Pilatz A., Veeratterapillay R., Köves B., Cai T., Bartoletti R., Wagenlehner F., et al. Update on Strategies to Reduce Infectious Complications After Prostate Biopsy Eur Urol Focus 2019 ;  5 (1) : 20-28 [cross-ref]
Ehdaie B., Vertosick E., Spaliviero M., Giallo-Uvino A., Taur Y., O'Sullivan M., et al. The Impact of Repeat Biopsies on Infectious Complications in Men with Prostate Cancer on Active Surveillance J Urol 2014 ;  191 (3) : 660-664 [cross-ref]
Loeb S., Carter H.B., Berndt S.I., Ricker W., Schaeffer E.M. Is Repeat Prostate Biopsy Associated with a Greater Risk of Hospitalization? Data from SEER-Medicare J Urol 2013 ;  189 (3) : 867-870 [cross-ref]
Panebianco V., Barchetti F., Manenti G., Aversa T., Catalano C., Simonetti G. MR imaging-guided prostate biopsy: technical features and preliminary results Radiol Med (Torino) 2015 ;  120 (6) : 571-578 [cross-ref]
Kasivisvanathan V., Rannikko A.S., Borghi M., Panebianco V., Mynderse L.A., Vaarala M.H., et al. MRI-Targeted or Standard Biopsy for Prostate-Cancer Diagnosis N Engl J Med 2018 ;  378 (19) : 1767-1777
Anastasiadis E., van der Meulen J., Emberton M. Hospital admissions after transrectal ultrasound-guided biopsy of the prostate in men diagnosed with prostate cancer: A database analysis in England: Complications after prostate biopsies Int J Urol 2015 ;  22 (2) : 181-186 [cross-ref]
Soeterik T.F.W., van Melick H.H.E., Dijksman L.M., Stomps S., Witjes J.A., van Basten J.P.A. Nerve Sparing during Robot-Assisted Radical Prostatectomy Increases the Risk of Ipsilateral Positive Surgical Margins J Urol 2020 ;  204 (1) : 91-95 [cross-ref]
Kinsella N., Helleman J., Bruinsma S., Carlsson S., Cahill D., Brown C., et al. Active surveillance for prostate cancer: a systematic review of contemporary worldwide practices Transl Androl Urol 2018 ;  7 (1) : 83-97 [cross-ref]
Mottet N., Bellmunt J., Briers E., Bolla M., Bourke L., Cornford P., De Santis M., Henry A., Joniau S., Lam T., Mason M.D., Van den Poel H., Van den Kwast T.H., Rouvière O., Wiegel T. Members of the EAU-ESTRO-ESUR-SIOG Prostate Cancer Guidelines Panel. EAU-ESTRO-ESUR-SIOG Guidelines on Prostate Cancer.
Klotz L., Pond G., Loblaw A., Sugar L., Moussa M., Berman D., et al. Randomized Study of Systematic Biopsy Versus Magnetic Resonance Imaging and Targeted and Systematic Biopsy in Men on Active Surveillance (ASIST): 2-year Postbiopsy Follow-up Eur Urol 2020 ;  77 (3) : 311-317 [cross-ref]






© 2020 
Elsevier Masson SAS. Tous droits réservés.