When Prostate Cancer Circulates in the Bloodstream
Abstract
:1. Introduction
2. Circulating and Disseminating Tumor Cells
2.1. CTC Biology
Circulating Tumor Materials | How do They Circulate in the Bloodstream | Main Properties | How to Detect Them | Main Results in Prostate Cancer |
---|---|---|---|---|
Circulating tumor cells (CTCs) | Isolated cells Cell clusters Cell fragments | Epithelial-to-mesenchymal transition Plasticity (organ mimicry) Resistance to anoikis Immune cell escape Ability to initiate metastases | 3 steps: Enrichment Tumor cell staining or oncogene probing Detection The FDA-approved CellSearch system is the most used method. Can be evaluated: CTC count (cutoff 5 CTCs/7.5 mL) Specific expression patterns Functional properties (ex: ELISPOT) | Poor ability of CTC count to diagnose early PCa Inconstant correlations between CTC counts and tumor burden, pN status, pM status Frequent correlation between CTC count and overall survival Evaluation of CTC count under treatment would be predictive of disease progression CTC count could be used as a surrogate marker of survival in clinical trials |
Extracellular vesicles (EVs) | Apoptotic bodies Microvesicles Exosomes | Intercellular trafficking Biologically significant cargo: proteins, lipids nucleic acids Ability to influence the biology of target cells | Centrifugation-based purification With difficulties | Mostly exosomes have been studies PCa cells produce exosomes Numerous specific or high throughput analyses of exosome contents have been performed No immediate transfer into clinical practice |
DNAs | Cell-free Mostly short fragments (apoptotic release) In plasma or serum | Reliable markers of intrinsic tumor biology | Mostly PCR-based methods Whole sequencing No standardization to date Can be evaluated: Whole DNA levels Targeted genetic alterations Whole genetic alterations DNA integrity Epigenetic events (methylation) | Extreme variations in the design of the published studies Contradictory results when evaluated for either diagnostic or prognostic purposes High potential interest to predict response to treatment and to personalize the treatment |
microRNAs (miRs) | Mostly as exosomal constituents Bound to high-density lipoproteins Bound to Ago2 protein | Strong association between miR and exosomal maturation processes Ability to influence the biology of target cells | Mostly RT-PCR-based methods Whole sequencing | Deregulation of several miRs has been associated with PCa risk, aggressiveness, staging and outcome miR-141 is one the most studied miRs No immediate transfer into clinical practice |
2.2. Methods to Detect CTCs and DTCs and Their Application to Prostate Cancer
2.3. Diagnostic and Prognostic Value of CTC Enumeration in Prostate Cancer
References | Technique for CTC Detection | Prostate Cancer Group | Control Group | Results |
---|---|---|---|---|
[37] | Immunomagnetic separation followed by cytokeratin and PSMA IHC | n = 25 patients with mPCa | n = 63 healthy controls | No CTC in healthy controls CTCs in 72% of the PCa patients |
[38] | Immunomagnetic separation followed by FACS | n = 10 patients with lPCa n = 10 patients with mPCa | n = 22 healthy controls | Higher CTC counts in patients with lPCa or mPCa than in healthy controls |
[47] | Immunomagnetic separation followed by cytokeratin IHC | n = 60 PCa, most of them before RP | n = 20 healthy controls | No CTC in healthy controls CTCs in 38% of the PCa patients |
[52] | Immunomagnetic separation followed by RT-PCR (PSA) | n = 284 PCa including:
| n = 52 healthy controls n = 51 men with elevated PSA levels and negative prostate biopsies or TURP n = 32 patients with other cancers | CTCs in:
|
[41] | Elispot | n = 24 patients with lPCa (12 before and 12 after treatment) n = 24 patients with mPCa | n = 31 patients with BPH or acute prostatitis n = 35 patients without prostate pathology n = 8 healthy controls | No CTC in non-PCa patients Test more frequently positive in the 24 mPCa (83%) than in the 12 lPCa before treatment (42%) No CTC in the 12 lPCa after treatment |
[53] | CellSearch | n = 84 patients with advanced PCa (130 samples) | n = 39 healthy controls | <2 CTCs/7.5 mL in healthy controls ≥2 CTCs/7.5 mL in 62% of the 130 cancer samples |
[54] | Immunomagnetic separation followed by RT-PCR (PSA) | n = 371 PCa including:
| n = 78 healthy controls n = 63 men with elevated PSA levels and negative prostate biopsies or TURP | CTCs in:
|
[51] | CellSearch | n = 97 patients prior to RP | n = 25 men with elevated PSA levels and negative prostate biopsies | CTCs detected in 21% vs. 20% (PCa vs. control groups) |
[4] | CTC-Chip | n = 55 patients (including 19 patients with lPCa) | n = 17 healthy controls | CTCs detected in 8/17 healthy controls (max: 10 CTCs/7.5 mL) 8/19 patients with lPCa had ≥14 CTCs |
[55] | CTC-Chip (herringbone Chip) | n = 15 patients with mPCa | n = 10 healthy controls | 0 to 8 CTCs/7.5mL on healthy controls ≥12 CTCs in 14 of the mPCa patients |
[50] | CellSearch | n = 26 patients with lPCa | n = 30 healthy controls | 3 healthy controls with 1 CTC/7.5 mL No difference for the mean CTC counts |
[56] | CellSearch | n = 26 patients with PCa and biochemical recurrence after RP | n = 7 healthy controls | No CTC in healthy controls CTCs in 73% of the PCa patients |
[49] | CellSearch | n = 20 patients with lPCa and high recurrence risk | n = 15 healthy controls | No difference for the mean CTC counts |
Reference | Patients | Methods | Correlations | ||||||
---|---|---|---|---|---|---|---|---|---|
Positive Correlation | Negative Correlation | No Correlation | Treatment | Metastases Status | |||||
Lower CTC Count | Higher CTC Count | Lower CTC Count | Higher CTC Count | ||||||
[38] | n = 10 mPCa | IM/FACS | Disease progression | - | - | - | - | - | |
[47] | n = 60 PCa | IM/IHC | Tumor stage | - | - | - | - | - | |
[52] | n = 284 PCa | IM/RT-PCR | Tumor burden | - | - | - | - | - | |
[53] | n = 85 advanced PCa | CellSearch | PSA; AP; LDH | Hb Creatinine | Gleason score | Androgen-depletion alone | Androgen-depletion and chemotherapy | No difference | |
[41] | n = 24 lPCa and 24 mPCa | Elispot | - | - | - | For the lPCa: | lPCa | mPCa | |
No treatment | Treatment | ||||||||
[72] | n = 41 CRPC | IM/FACS | PSA; AP | Age | LDH; Hb; ECOG status | No difference when comparing the number of previous treatments | - | - | |
[58] | n = 112 mPCa | CellSearch | PSA; Bone metastases burden | - | - | No chemotherapy | Chemotherapy | Soft tissue only | Bone or Bone and soft tissue |
[54] | n = 371 PCa | IM/RT-PCR | PSA | - | Gleason score; Tumor stage; Resection margins; pN status | - | - | - | - |
[4] | n = 19 lPCa | CTC-Chip | - | - | PSA; Gleason score; Tumor size; Extracapsular extension; pN status; Perineural invasion; Resection margins | - | - | - | - |
[24] | n = 16 CRPC | Adnagen | Radiological response | - | - | No disease progression under treatment | Disease progression under treatment | - | - |
[56] | n = 26 PCa with rising PSA after RP | CellSearch | - | - | PSA | - | - | - | - |
[50] | n = 26 lPCa | CellSearch | pN status; PSA; Tumor size | - | Gleason score | - | - | No metastases | Metastasis |
[64] | n = 21 | Adnagen | Disease progression | - | - | Disease controlled under treatment | Disease not controlled under treatment | - | - |
[60] | n = 202 PCa | CellSearch | PSA; Gleason score | - | - | Non androgen-depleted | Androgen-depleted | Lymph node only | Bone or Bone and lymph node |
[49] | n = 41 CRPC | CellSearch | AP; LDH | Hb;PSADT | PSA; Calcemia; Bone metastatic burden | - | - | Soft tissue only | Bone or Bone and soft tissue |
Reference | Clinical Situation | Number of Patients | Methods | Use of CTC Count | CTC count as Predictor of overall Survival | Remark |
---|---|---|---|---|---|---|
[73] | mPCa | n = 37 | IM/FACS | Continuous variable | Yes Independently | Similar results for a subgroups of 26 CRPC |
[72] | CRPC | n = 41 | IM/FACS | Binary variable (cutoff: 1.8) | Yes | Cutoff 1.8 was considered as the best cutoff to separate patients with favorable or unfavorable survival outcome |
[58] | mPCa | n = 112 | CellSearch | Continuous variable | Yes Independently | - |
[69] | CRPC | n = 231 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | Part of the IMMC38 trial CTC counts at 2–5 weeks were also predictors |
[74] | CRPC before docetaxel | n = 164 | CellSearch | Continuous variable | Yes Independently | Part of the IMMC38 trial (same patients than [69]) CTC counts at 4, 8 and 12 weeks were also predictors |
[62] | CRPC | n = 51 | CellSearch | - | Yes | - |
[70] | CRPC | n = 64 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | - |
[68] | CRPC | n = 119 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | - |
[75] | CRPC | n = 100 | CellSearch | Binary variable (cutoff: 4) | Yes Independently | Cutoff 4 was considered as the best cutoff to separate patients with favorable or unfavorable survival outcome |
[76] | CRPC before docetaxel | n = 179 | CellSearch | Continuous variable | Yes | Part of the IMMC38 trial (same patients than [69]) |
[67] | CRPC | n = 76 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | - |
[59] | CRPC | n = 162 | CellSearch | Binary variable (cutoff: 5) | Yes | Part of the IMMC38 trial (same patients than [69]) |
[50] | mPCa | n = 27 | CellSearch | Binary variable (cutoff: 4) | Yes | CTC enumeration was also predictive of disease progression-free survival |
[60] | PCa | n = 202 | CellSearch | Binary variable (cutoff: 5) | Yes | - |
[49] | CRPC | n = 55 | CellSearch | Binary variable (cutoff: 5) | Yes | Best calculated cutoff to predict overall survival: 3 CTCs/7.5 mL) |
Continuous variable | Yes | |||||
[66] | CRPC | n = 57 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | - |
[61] | CRPC | n = 238 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | Part of the SWOG SO42 trial |
[65] | Previously docetaxel-treated CRPC | n = 711 | CellSearch | Binary variable (cutoff: 5) | Yes Independently | Part of the COO-AA-301 trial Combination of CTC counts with LDH levels was also a good predictor of overall survival |
2.4. Molecular Characterization of Prostate CTCs and Prediction of Treatment Response
2.5. Circulating Tumor Emboli (CTC Clusters or Aggregates)
3. Other Circulating Tumor Cellular Materials
3.1. Circulating Vesicles
Extracellular Vesicles | Size Range | Production | Cell of Origin | Markers |
---|---|---|---|---|
Apoptotic bodies | 0.5–5 mm | During the late stage of apoptosis | All cell types | Expression of phosphatidylserine on the membrane surface |
Microvesicles (or microparticles or ectosomes) | 0.2–1 mm | Outward protrusion/budding from the plasma membrane | Tumor cells Polynuclear leukocytes Aging erythrocytes | Expression of phosphatidylserine on the membrane surface |
Exosomes | 40–100 nm | Endosome-derived Liberation by fusion with the plasma membrane | Probably all cell types | Alix TSG101 Tetraspanins Heat shock proteins |
3.2. Circulating Nucleic Acids
3.2.1. Circulating DNA
Reference | Number of PCa | Number of Controls | Fluid | Method | Results for Circulating DNA Levels |
---|---|---|---|---|---|
[152] | 91 | 34 BPH 59 healthy controls | P | FA | No difference between lPCas and controls N1M1 PCa and BPH Patients with mPCa under ADT or not No correlation between DNA levels and PSA, pT, Gleason in pN0M0 PCa Correlation between DNA levels and PSA in M1 PCas Correlation between DNA levels and overall survival |
[187] | 12 | 13 | P | RT-PCR | Se = 58%; Spe = 92%; AUC = 0.708 |
[154] | 15 | 10 BPH 12 HGPIN | P | RT-PCR | Increase in DNA levels after prostate biopsies No difference between PCa and HGPIN When comparing PCa + HGPIN vs. BPH: Se = 85% ; Spe = 73% |
[157] | 78 | 15 patients with low PCa risk a 74 patients with negative biopsies 10 healthy controls | P | RT-PCR | Increase in DNA levels in PCa vs. the 15 patients with negative biopsies and the 10 healthy controls Increase in DNA levels in the 74 with negative biopsies vs. the 78 PCa patients |
[153] | 12 newly diagnosed PCa 15 PCa subjected to treatment | 13 healthy controls | P | RT-PCR | Increase in DNA levels in newly diagnosed PCa vs. the healthy controls No difference in PCa patients subjected to treatment and healthy controls No correlation between DNA levels and Gleason score |
[150] | 61 | 62 | P | RT-PCR | No difference between the two groups |
[159] | 142 lPCa | 19 BPH | P | SA | Increase in DNA levels in PCa patients Increase in predictive accuracy when DNA levels are added to a base model |
[156] | 192 lPCa 18 mPCa | 35 patients with negative biopsies | S | RT-PCR | Increase in DNA levels in: mPCa patients vs. the lPCa patients lPCa patients with PSA recurrence vs. lPCA without PSA recurrence In lPCa patients, correlation between DNA levels and Gleason at biopsy, Gleason at prostatectomy, positive surgical margins and pT |
[140,177] | 168 lPCa 5 incidental PCa b | 42 BPH 11 healthy controls | S | RT-PCR | When comparing the 168 lPCa to the 42 BPH : Se = 88%, Spe = 64% and AUC = 0.824 |
[155] | 64 | 45 healthy controls | P | RT-PCR | Increase in DNA levels in PCa patients Se = 80%, Spe = 82% and AUC = 0.881 Correlation between DNA levels and pT No correlation between DNA levels and Gleason or PSA |
[151] | 5 | 22 BPH 30 healthy controls | P | FA | No difference between PCa and BPH |
[144] | 69 lPCa 12 mPCa | 10 healthy controls | P | SA | Increase in DNA levels: in mPCa patients vs. lPCa patients in mPCa patients vs. healthy controls No difference between lPCa patients and healthy controls |
[161] | 89 | 104 BPH 59 prostatitis | S | RT-PCR | Increase in DNA levels: in PCa patients vs. BPH patients in PCa patients vs. BPH and prostatitis patients No difference between BPH patients and prostatitis patients No correlation between DNA levels and Gleason score Increase in predictive accuracy when DNA levels are added to a base model |
[164] | 8 CRPC | - | P | RT-PCR | Increase in DNA levels after docetaxel therapy No correlation between DNA levels and PSA Correlation between DNA levels and tumor activity at PET/CT imaging |
[141] | 19 | 20 healthy controls | P | RT-PCR | Increase in DNA levels after 3 month ADT or 3 months after surgery No correlation between DNA levels and Gleason, PSA doubling time or PSA recurrence |
[160] | 96 | 112 BPH | P | RT-PCR | Increase in DNA levels in PCa patients Correlation between DNA levels and PSA or Gleason |
[163] | 133 | 33 patients with negative biopsies | P | SA | Increase in DNA levels in PCa patients Se = 66%, Spe = 88% No correlation between DNA levels and PSA, Gleason, pT, or BRFS Correlation between an increase in DNA levels during the follow up (sampling every 3 months during 2 years) and BRFS |
[162] c | 85 | 101 BPH 55 prostatitis | S | FA | Increase in DNA levels in PCa patients Increase in predictive accuracy when DNA levels are added to a base model |
[158] | 16 | 25 BPH 40 healthy controls | P | FA | No difference between PCa and BPH Increase in the ratio cell-free/total circulating DNA in PCa and BPH patients vs. healthy controls |
Reference | Number of PCa | Number of Controls | Fluid | Method | Studied Gene(s) | Results | |||
---|---|---|---|---|---|---|---|---|---|
[174] | 33 | 26 BPH | S & P | MSP | GSTP1 | Se = 72%; Spe = 100% | |||
[180] | 7 | - | S | MSP | CD44 | Se = 100% No correlation with the pM status Physiologic hypermethylation in several normal epithelia | |||
[175] | 85 lPCa 18 CRPC | 35 patients with negative biopsies | S | qMSP | GSTP1 | Spe = 100% Se = 12% in lPCa patients and 28% in CRPC (p = 0.003) Correlation with biochemical recurrence and BRFS | |||
110 patients with RP 55 with recurrence 55 without recurrence | - | S | qMSP | GSTP1 | GSTP1 methylation in 8 patients with recurrence and none of the patients without recurrence | ||||
[153] | 31 | 9 healthy controls | P | MSP | GSTP1 | Se = 52%; Spe = 100% | |||
[178] | 14 lPCa 62 CRPC | 49 healthy controls | S | MSP | - GSTP1 AR 14-3-3β | Healthy 0 27% 55% | lPCa 21% 36% 86% | CRPC 32% 40% 87% | Significant increase for GSTP1 Correlation between GSTP1 methylation and Gleason, pM and pN status No correlation between GSTP1 and PSA, overall survival, response to treatment |
[176] | 36 | 27 BPH | P | MSP | GSTP1 | Se = 31% ; Spe = 93% | |||
[181] | 192 lPCa 18 CRPC | 35 patients with negative biopsies | S | qMSP | Several genes including MDR1 | MDR1 was the only hypermethylated promoter in lPCa: 16% of the patients without biochemical recurrence 38% of the patients with biochemical recurrence IN CRPC patients, hypermethylation in MDR1 (89%), EDNRB (50%), RARβ (39%) | |||
[188] | 5 | 5 BPH 5 healthy controls | P | MSP and sequencing | GSTP1 | Sequencing provided different methylation patterns according to pathological diagnosis. | |||
[177] | 168 PCa 5 incidental PCa | 42 BPH 11 healthy controls | S | MSP | - GSTP1 TIG1 PTGS2 Reprimo | BPH 8% 0 0 0 | PCa 42% 10% 2% 1% | GSTP1 methylation in 4 of the 5 incidental PCas Significant difference between BPH and PCa for GSTP1 and TIG1 No correlation between methylation and pT, Gleason or biochemical recurrence | |
[179] | 20 PCa with disease progression 22 PCa without disease progression | 22 BPH | Whole blood | qMSP | Several including GSTP1 RASSF1a APC RARβ | BPH 9% 23% 9% 9% | Not recurring PCa 91% 95% 91% 68% | Recurring PCa 100% 100% 95% 90% | Significant increase with PCa and disease progression. |
[182] | 2 PCa stage II 1 PCa stage III 1 PCa stage IV | 1 BPH | S | MSP | Gal3 | No Gal3 hypermethylation on the BPH patient and in the stage III and IV patients The 2 patients with stage II PCa exhibited Gal3 hypermethylation | |||
[170] | 83 | 40 healthy | S | MSP | GSTP1 RASSF1 RARβ2 | 12% 24% 13% | None of the healthy controls exhibited hypermethylation At least one hypermethylation in 28% of the PCa patients Correlation between the presence of at least one hypermethylation and PSA, Gleason score and stage | ||
[183] | 22 lPCa 11 locally advanced PCa 28 mPCa | - | P | ELISA | H3K27me3 (trimethylated histone H3 lysine 27) | The median plasma level of H3K27me3 was significantly lower in mPCa than in lPCa and locally advanced PCa | |||
[186] | 19 PCa | 20 BPH 20 healthy controls | P | Micro-array | Global profiling | In this exploratory set, no difference in the methylation patterns between PCa and BPH 39 PCa-associated changes when compared to healthy controls; 7 out of them were confirmed by sequencing, including RNF219 Diagnostic performances of RNF219: Se = 89%, Spe = 71%, AUC = 0.79 | |||
20 Pca | 18 BPH | P | PS | RNF219 | In this validation set, the diagnostic performances of RNF219: Se = 61%, Spe = 71%, AUC = 0.56 | ||||
[146] | 75 CRPC before chemotherapy | - | P | qMSP | GSTP1 | No correlation with Gleason score, bone metastasis status or PSA response to treatment GSTP1 hypermethylation was an independent predictor of overall survival Correlation between methylated GSTP1 levels after the first chemotherapy cycle and PSA progression | |||
[184] | 98 | 27 BPH 9 healthy controls 11 bladder stone | S | MSP | CDH13 | Se = 45%; Spe = 100% Correlation with Gleason score, pT, and PSA CDH13 methylation status was an independent predictor of overall survival | |||
[189] | 694 | 703 | P | PS | Line1 Alu | Iterative samples as part of the Prostate, Lung, Colorectal and Ovarian cancer screening trial No correlation with PCa or PCa aggressiveness Variations were observed for Alu methylation status depending on the time between blood sampling and PCa diagnosis | |||
[185] | 34 | 48 | S | PS | GADD45a | Higher levels in PCa patients No correlation with Gleason score |
3.2.2. Circulating MicroRNAs
Reference | Number of PCa Patients | Number of Controls | microRNAs Found to be Deregulated in Peripheral Blood | Remarks |
---|---|---|---|---|
[200] | 25 patients with mPCa | 25 healthy controls | miR-100, -125b, -141, -143, and -296 | miR-141 was the most significantly increased |
[202] | 5 patients with PCa | 8 healthy controls | miR-16, -92a, -103, -107, -197, -34b, -328, -485-3p, -486-5p, -92b, -574-3p, -636, -640, -766, ans -885-5p | Several patients were pre-treated with chemotherapy |
[203] | 36 patients with PCa | 12 healthy controls | miR-223, -26b, -30c, -24, -874, -1247a, -1207-5p, -93, and -106a | miR-24 and miR-106a decreased and increased with PCa aggressiveness, respectively |
[204] | 51 patients with PCa | 20 healthy controls | miR-21 and -221 | miR-141 was also elevated when considering only mPCa |
[205] | 21 patients with mPCa | - | miR-141 | Correlation with clinical progression and PSA |
[206] | 50 patients with PCa | 6 patients with BPH | miR-21 | Elevation only on patients with CRPC and patients with hormone-sensitive mPCa Higher levels in patients with resistance to docetaxel |
[207] | 21 patients with PCa | - | miR-375, -9*, -141, -200b, and -516a-3p | - |
116 patients with PCa | - | miR-375 and -141 | Higher levels in high-risk patients (Gleason score ≥ 8 or metastases) Higher levels of both miR in patients with positive lymph nodes. | |
[208] | 25 Patients with CRPC | 25 healthy controls | miR-141, -298, -246, and -375 | - |
[209] | 70 Patients after surgery | - | miR-141, -146b-3p, and -194 | Prediction of biochemical resistance following radical prostatectomy |
[210] | 78 patients with PCa | 28 healthy controls | miR-107, -130b, -141, -2110, -301a, -326, -331-3p, -432, -484, -574-3p, -181a-2, and -625 | miR were evaluated within circulating exosomes and larger microvesicles Higher levels of miR-221, - 375, and -141 in patients with mPCa as compared to non-metastatic patients |
[211] | 23 Patients with CRPC | - | miR-375 and -1290 | miR were evaluated within circulating exosomes |
[212] | 84 patients with PCa | - | miR-375, -378, 409-3p, and -141 | Higher levels in CRPC patients than in patients with lPCa |
[213] | 25 patients with PCa | 17 patients with BPH | miR-let-7e, -let-7c, -30c, -622, and -1285 | - |
[214] | 82 patients with PCa | - | miR-20a, -21, -145, and -221 | Smaller levels in patients with lPCa |
[215] | 45 patients with PCa | 18 patients with BPH and 20 healthy controls | miR-26a, -195, and let-7i | - |
[216] | 54 patients with positive prostate biopsies | 79 patients with negative prostate biopsies | miR-26a-1 and -141 | Diagnostic cohort of 133 patients undergoing prostate biopsies No difference in miR levels in the 2 groups Increased levels of miR-141 with increasing Gleason score in patients with positive biopsies |
[217] | 75 patients with positive prostate biopsies | 27 patients with negative prostate biopsies | miR-let7a, -141, -145, and -155 | Higher miR-141 levels with d’Amico’s classification |
[218] | 150 patients with PCa prior to surgery | 50 patients with BPH | Combination of expression levels of 14 miRNAs into a “miR Score” | Lower levels in high-risk cancer |
[219] | 97 patients with CRPC | - | miR-200b and -20a | Correlation with overall survival |
[220] | 59 patients with PCa | 16 patients with BPH and 11 healthy controls | miR-375 and –let-7c | Higher diagnostic performances when the two miR were combined. |
[221] | 31 patients with PCa | 13 patients with BPH | miR-375 and -141 | Higher diagnostic performances when the two miR were combined. |
4. Conclusion
Conflicts of Interest
References
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Vlaeminck-Guillem, V. When Prostate Cancer Circulates in the Bloodstream. Diagnostics 2015, 5, 428-474. https://doi.org/10.3390/diagnostics5040428
Vlaeminck-Guillem V. When Prostate Cancer Circulates in the Bloodstream. Diagnostics. 2015; 5(4):428-474. https://doi.org/10.3390/diagnostics5040428
Chicago/Turabian StyleVlaeminck-Guillem, Virginie. 2015. "When Prostate Cancer Circulates in the Bloodstream" Diagnostics 5, no. 4: 428-474. https://doi.org/10.3390/diagnostics5040428
APA StyleVlaeminck-Guillem, V. (2015). When Prostate Cancer Circulates in the Bloodstream. Diagnostics, 5(4), 428-474. https://doi.org/10.3390/diagnostics5040428