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| Cell-free DNA in the management of prostate cancer: Current status and future prospective |
Wei Hea,Yutian Xiaob,Shi Yanb,c,Yasheng Zhub,d,*( ),Shancheng Rend,*()
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a College of Basic Medical Sciences, Naval Medical University, Shanghai, China
b Department of Urology, The First Affiliated Hospital, Naval Medical University, Shanghai, China
c Department of Urology, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University, Shanghai, China
d Department of Urology, The Second Affiliated Hospital, Naval Medical University, Shanghai, China |
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Abstract Objective With the escalating prevalence of prostate cancer (PCa) in China, there is an urgent demand for novel diagnostic and therapeutic approaches. Extensive investigations have been conducted on the clinical implementation of circulating free DNA (cfDNA) in PCa. This review aims to provide a comprehensive overview of the present state of cfDNA as a biomarker for PCa and to examine its merits and obstacles for future clinical utilization.
Methods Relevant peer-reviewed manuscripts on cfDNA as a PCa marker were evaluated by PubMed search (2010-2022) to evaluate the roles of cfDNA in PCa diagnosis, prognosis, and prediction, respectively.
Resultsc fDNA is primarily released from cells undergoing necrosis and apoptosis, allowing for non-invasive insight into the genomic, transcriptomic, and epigenomic alterations within various PCa disease states. Next-generation sequencing, among other detection methods, enables the assessment of cfDNA abundance, mutation status, fragment characteristics, and epigenetic modifications. Multidimensional analysis based on cfDNA can facilitate early detection of PCa, risk stratification, and treatment monitoring. However, standardization of cfDNA detection methods is still required to expedite its clinical application.
Conclusionc fDNA provides a non-invasive, rapid, and repeatable means of acquiring multidimensional information from PCa patients, which can aid in guiding clinical decisions and enhancing patient management. Overcoming the application barriers of cfDNA necessitates increased data sharing and international collaboration.
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Received: 03 August 2022
Available online:
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Corresponding Authors:
Yasheng Zhu,Shancheng Ren
E-mail: zys0562@foxmail.com;renshancheng@gmail.com
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An overview of the molecular information derived from cfDNA and its clinical applications. cfDNA is originated from apoptotic or necrotic cells. Neutrophils can also release extracellular traps as part of a controlled cell-death process. Alive cells are also able to release cfDNA actively. cfDNA shedding into blood stream, urine, or other body fluids can be used to measure its abundance, mutation status, epigenetic changes, and altered fragmentation pattern. cfDNA could be potentially applied in several clinical aspects, including screening, early detection, prognostic assessment, risk prediction of recurrence and metastasis. Future clinical applications also include monitoring treatment response, identifying mechanism of resistance and minimal residual identification. cfDNA, circulating cell-free DNA. This figure was created with BioRender.com (BioRender, Toronto, Canada).
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Proposed pipelines of cfDNA in the clinical management of prostate cancer. PSA test identified suspicious population from general population. Further cfDNA test discovered high-risk population. Biopsy-confirmed prostate cancer patients further underwent individualized risk assessment and treatment method selection. For active surveillance patients, cfDNA severed as real-time monitoring and helped to decide to continue active surveillance or be transferred to other therapies. cfDNA could warn early recurrence and cfDNA-guided precision medicine could identify key molecular alterations to guide clinical decision-making and long-term follow-up. cfDNA, circulating cell-free DNA; PSA, prostate-specific antigen. This figure was created with BioRender.com (BioRender, Toronto, Canada).
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Clinical applications of cfDNA in the management of advanced or recurrent or progressed prostate cancer. Molecular alterations derived from urine or blood cfDNA have high concordance with tissue biopsy and can overcome tumor heterogeneity limited by multi-tumor or metastasis foci. Specific genetic variations defined different molecular subtypes. For example, prostate cancer with loss of functions alterations in DNA damage repair pathways unveiled by cfDNA analysis often suggests more aggressive clinical and pathological characteristics. These patients were more suitable to be treated with PARP inhibitors while they were more likely to be resistant to anti-androgen therapy. cfDNA, circulating cell-free DNA; ICI, immune checkpoint inhibitor; OS, overall survival; AR, androgen receptor; AR V7(+), androgen receptor splice variant 7 (positive); CDK12, cyclin dependent kinase 12; PARP, poly adenosine diphosphate ribose polymerase; BRCA2, breast cancer susceptibility genes 2; ATM, ataxia telangiectasia-mutated gene. This figure was created with BioRender.com (BioRender, Toronto, Canada).
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| Reference | Cohort (n) | Resource | Results | Method | | Hennigan et al., 2019 [58] | ·-
Localized PCa (112) | ·Plasma | - Low abundance of cfDNA in localized PCa | ULP WGS | | Chen et al., 2021 [85] | ·-
HD (34) | ·Plasma (7-55 mL) | - cfDNA fragment size may be an alternative that can differentiate PCa patients from HD | Quantitative real-time PCR | ·-
Localized PCa (112) | ·-
mCRPC (122) | | Salvi et al., 2015 [96] | ·-
PCa (67) | ·Urine (30 mL) | - UCF-DNA integrity showed lower accuracy than PSA for early PCa diagnosis | Quantitative real-time PCR | ·-
Benign diseases of the urogenital tract (64) | | Constancio et al., 2019 [73] | ·-
Lung cancer (102) | ·Plasma | - Methylation analysis of FOXA1, RARβ2, RASSF1A, GSTP1, and SOX17 facilitated early detection of PCa | WGBS | ·-
PCa (121) | ·-
Colorectal cancer (100) | ·-
HD (136) | | Bryzgunova et al., 2021 [74] | ·-
PCa (20) | ·Plasma (2 mL) | - GSTP1 and RNF219 gene methylation analysis differentiated PCa patients from HD | Locus-specific NGS | ·-
HD (18) | ·-
BPH (17) | | Tomeva et al., 2022 [75] | ·-
PCa (27) | ·Plasma | - Androgen receptor mutation p.H875Y associated with cfDNA methylation and circulating miRNAs to distinguish PCa patients from HD | Quantitative real-time PCR | ·-
HD (15) | | Cario et al., 2020 [90] | ·-
PCa (550) | ·Public data from the ICGC | - Optimizing cfDNA mutation detection performance based on machine learning | Using machine learning to optimize targeted sequencing panels | | Brikun et al., 2019 [93] | ·-
Patients with elevated PSA (94) | ·Urine | - Methylation of HOXD3, HOXA7, GPR62, and KLK10 were candidates for early detection markers of PCa | Semi-quantitative PCR | | Chen et al., 2021 [91] | ·-
Localized PCa (21) | ·Plasma | - Targeted cfDNA sequencing identifies mutations in FOXA1, PTEN, MED12, and ATM to detect localized PCa | Targeted and low-pass WGS | ·-
HD (15) | ·-
mCRPC (9) |
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cfDNA in PCa screening and detection.
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| Reference | Cohort (n) | Resource | Results | Method | | Kubota et al., 2021 [101] | ·-
HD (47) | Plasma (1 mL) | ·-
High cfDNA and AR-amp-high were significantly associated with poor OS in CRPC | Quantitative real-time PCR | ·-
Localized PCa with ADT (57) | ·-
CSPC with ADT (97) | ·-
CRPC (97) | | Kohli et al., 2020 [103] | ·-
Independent patients (4; untreated mHSPC and mCRPC) | Plasma | ·-
TP53 mutation, RB1 loss, and AR gene amplification were associated with poor OS in mCRPC | NGS | | Lau et al., 2020 [128] | ·-
Localized PCa | Plasma | ·-
ctDNA TP53 mutations were associated with significantly shorter metastasis-free survival | WGS and TAm-Seq | | ·(prospectively; 8) | ·-
PCa | | ·(retrospective; 189) | | Bjerre et al., 2020 [50] | ·-
HD (36) | Plasma | ·-
Methylated ctDNA (DOCK2/HAPLN3/FBXO30) was associated with a significantly shorter time to progression or metastasis | MS-ddPCR | ·-
BPH (61) | ·-
Localized PCa (102) | ·-
Metastatic PCa (65) | | Del Re et al., 2021 [137] | ·-
mCRPC (84; 40 abiraterone, 44 enzalutamide) | Plasma (10 mL) | ·-
AR gain in cfDNA predicted resistance to AR signaling inhibitors | ddPCR | | Hussain et al., 2020 [146] | ·-
Olaparib (256 patients) | Plasma | ·-
At least one alteration in BRCA1, BRCA2, or ATM responded better to olaparib | NGS-based FoundationOne CDx (Foundation Medicine, USA) | ·-
Enzalutamide or abiraterone plus prednisone (131 patients) | | Reimers et al., 2020 [155] | ·-
Advanced PCa (317; 172 tumor tissue, 145 ctDNA) | Tissue and plasma | ·-
Patients with CDK12 mutant PCa exhibited a shorter time to metastasis | NGS | | Sumanasuriya et al., 2021 [159] | ·-
mCRPC (188) | Plasma | ·-
Longitudinal changes in ctDNA fraction enabled monitoring of drug response | lpWGS | | Beltran et al., 2020 [49] | ·-
Metastatic PCa (10) | Plasma | ·-
Combination of genomic (TP53, RB1, CYLD, and AR) and epigenomic alterations applied to ctDNA identifies patients with CRPC-NE | WES and WGBS | ·-
CRPC (35) | ·-
CRPC-NE (17) |
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cfDNA in PCa risk stratification and monitoring.
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| No. | ClinicalTrials.gov NCT number | Condition | Purpose | Status | Phase | | 1 | NCT04015622 | mCRPC | - PCa treatment optimization via analysis of ctDNA | Recruiting | Phase 2 | | 2 | NCT04601441 | mCSPC | - Evaluate changes in genomic alterations for 73 PCa driver genes during apalutamide treatment | Recruiting | Phase 4 | | 3 | NCT03228810 | Metastatic PCa | - Detect and calculate ctDNA in relation to metastasis-directed radiation and ADT | Completed | NA | | 4 | NCT05116579 | mCRPC | - Evaluate the application value of customized ctDNA monitoring in efficacy assessment and prediction during PARPi treatment | Recruiting | NA | | 5 | NCT03903835 | mCRPC | - Prolong progression-free survival by measuring ctDNA in plasma and adapting the treatment accordingly | Recruiting | Phase 3 | | 6 | NCT02771769 | Men with elevated PSA levels | - Determine whether copy number instability scores derived from the cfDNA correlates with PSA screening levels and prostate biopsy results | Terminated | NA | | 7 | NCT04081428 | Localized PCa | - Using breath, cfDNA, and image analysis to predict normal tissue and tumor response during PCa SBRT | Recruiting | NA | | 8 | NCT03385655 | mCRPC | - cfDNA helped predict which patients are most likely to be helped by the drugs | Recruiting | Phase 2 | | 9 | NCT04580667 | Untreated PCa | - Develop a new test of cfDNA to identify PCa patients at the highest risk of radiotherapy-related complications, especially those related to GI toxicities | Recruiting | NA | | 10 | NCT05245435 | Primary oligometastatic PCa | - Study the diagnostic and prognostic accuracy and health economics considerations of cfDNA | Recruiting | NA |
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Selective clinical trials of cfDNA or ctDNA in PCa.
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