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Liquid Biopsy: Current Status and Future Perspectives

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A special issue of Cancers (ISSN 2072-6694). This special issue belongs to the section "Cancer Causes, Screening and Diagnosis".

Deadline for manuscript submissions: closed (31 March 2023) | Viewed by 41110

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Dr. Danijela Koppers-Lalic

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Guest Editor

1. Department of Neurosurgery, Brain Tumor Center Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands
2. Amsterdam UMC, VU University Medical Center, Amsterdam, The Netherlands
Interests: RNA; liquid biopsy; next-generation sequencing; epi-transcriptomics; biomarkers

Prof. Dr. Vesselin Baev

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Guest Editor

Department of Molecular Biology, University of Plovdiv, 4000 Plovdiv, Bulgaria
Interests: bioinformatics; NGS; tool development; genomics; metagenomics; transcriptomics
Special Issues, Collections and Topics in MDPI journals

Dr. Bruno Costa Silva

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Guest Editor

Champalimaud Centre for the Unknown, Champalimaud Foundation, Lisbon, Portugal
Interests: tumor metastasis; tumor microenvironment; extracellular vesicles; liquid biopsy

Special Issue Information

Dear Colleagues,

Liquid biopsies have been heralded as a game-changer in cancer management, offering a minimally invasive, safe, and sensitive alternative or complementary approach for tissue biopsies. Although peripheral blood is the primary source of liquid biopsies, other biological fluids such as urine, saliva, and cerebrospinal fluid also represent a rich source of information through which solid cancers (and their subtypes) can be detected, identified, classified, and matched to a specific therapy. Currently, blood-based biopsy measurements focus on four main biomarker sources for cancer detection and stratification: circulating tumor DNA (ctDNA), circulating tumor cells (CTCs), tumor-educated platelets (TEPs), and extracellular vesicles (EVs). Additionally, tumor cells continuously release diverse nucleic acids (e.g., small non-coding RNAs) and proteins, which can be found in biological fluids and linked to the presence of cancer cells. This Special Issue aims to address current advances and hurdles in implementing liquid biopsy-based diagnostics in standard clinical practice. We are particularly interested in technical advances and novel approaches for the detection, isolation, and characterization of tumor-derived molecular material released in bodily fluids. These include improved sensitivity and specificity of assays, the application of advanced computational analyses, the incorporation of multi-modal analysis approaches, and the development of automatized protocols. Authors are encouraged to submit their original research studies concerning this topic. Reviews that highlight new findings in the above areas are also welcome.

Dr. Danijela Koppers-Lalic
Prof. Dr. Vesselin Baev
Dr. Bruno Costa Silva
Guest Editors

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Keywords

liquid biopsy
biomarkers
RNA
DNA
protein
extracellular vesicles
CTC
ctDNA
bioinformatics
biostatistics
assay development
plasma
serum
urine
CSF
saliva

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Published Papers (11 papers)

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Editorial

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3 pages, 173 KiB

Open AccessEditorial

Liquid Biopsy: Current Status and Future Perspectives

by Vesselin Baev, Danijela Koppers-Lalic and Bruno Costa-Silva

Cancers 2023, 15(12), 3205; https://doi.org/10.3390/cancers15123205 - 15 Jun 2023

Cited by 4 | Viewed by 1942

Abstract

Since the discovery of the Bence Jones protein in the middle to late 1800s and the subsequent identification of the carcinoembryonic antigen and alpha-fetoprotein in the 1970s, it has been demonstrated that the analysis of biofluids is essential to the diagnostic and follow-up [...] Read more.

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

Research

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20 pages, 1881 KiB

Open AccessArticle

Simultaneous Ultra-Sensitive Detection of Structural and Single Nucleotide Variants Using Multiplex Droplet Digital PCR in Liquid Biopsies from Children with Medulloblastoma

by Cecilia Arthur, Cecilia Jylhä, Teresita Díaz de Ståhl, Alia Shamikh, Johanna Sandgren, Richard Rosenquist, Magnus Nordenskjöld, Arja Harila, Gisela Barbany, Ulrika Sandvik and Emma Tham

Cancers 2023, 15(7), 1972; https://doi.org/10.3390/cancers15071972 - 25 Mar 2023

Cited by 8 | Viewed by 2606

Abstract

Medulloblastoma is a malignant embryonal tumor of the central nervous system (CNS) that mainly affects infants and children. Prognosis is highly variable, and molecular biomarkers for measurable residual disease (MRD) detection are lacking. Analysis of cell-free DNA (cfDNA) in cerebrospinal fluid (CSF) using broad genomic approaches, such as low-coverage whole-genome sequencing, has shown promising prognostic value. However, more sensitive methods are needed for MRD analysis. Here, we show the technical feasibility of capturing medulloblastoma-associated structural variants and point mutations simultaneously in cfDNA using multiplexed droplet digital PCR (ddPCR). Assay sensitivity was assessed with a dilution series of tumor in normal genomic DNA, and the limit of detection was below 100 pg of input DNA for all assays. False positive rates were zero for structural variant assays. Liquid biopsies (CSF and plasma, n = 47) were analyzed from 12 children with medulloblastoma, all with negative CSF cytology. MRD was detected in 75% (9/12) of patients overall. In CSF samples taken before or within 21 days of surgery, MRD was detected in 88% (7/8) of patients with localized disease and in one patient with the metastasized disease. Our results suggest that this approach could expand the utility of ddPCR and complement broader analyses of cfDNA for MRD detection. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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25 pages, 2345 KiB

Open AccessArticle

Comprehensive Analysis of Serum Small Extracellular Vesicles-Derived Coding and Non-Coding RNAs from Retinoblastoma Patients for Identifying Regulatory Interactions

by Radhika Manukonda, Vengala Rao Yenuganti, Nupur Nagar, Pankaj Singh Dholaniya, Shivani Malpotra, Jyothi Attem, Mamatha M. Reddy, Saumya Jakati, Dilip K Mishra, Pallu Reddanna, Krishna Mohan Poluri, Geeta K. Vemuganti and Swathi Kaliki

Cancers 2022, 14(17), 4179; https://doi.org/10.3390/cancers14174179 - 29 Aug 2022

Cited by 7 | Viewed by 3061

Abstract

The present study employed nanoparticle tracking analysis, transmission electron microscopy, immunoblotting, RNA sequencing, and quantitative real-time PCR validation to characterize serum-derived small extracellular vesicles (sEVs) from RB patients and age-matched controls. Bioinformatics methods were used to analyze functions, and regulatory interactions between coding and non-coding (nc) sEVs RNAs. The results revealed that the isolated sEVs are round-shaped with a size < 150 nm, 5.3 × 10¹¹ ± 8.1 particles/mL, and zeta potential of 11.1 to −15.8 mV, and expressed exosome markers CD9, CD81, and TSG101. A total of 6514 differentially expressed (DE) mRNAs, 123 DE miRNAs, and 3634 DE lncRNAs were detected. Both miRNA-mRNA and lncRNA-miRNA-mRNA network analysis revealed that the cell cycle-specific genes including CDKNI1A, CCND1, c-MYC, and HIF1A are regulated by hub ncRNAs MALAT1, AFAP1-AS1, miR145, 101, and 16-5p. Protein-protein interaction network analysis showed that eye-related DE mRNAs are involved in rod cell differentiation, cone cell development, and retinol metabolism. In conclusion, our study provides a comprehensive overview of the RB sEV RNAs and regulatory interactions between them. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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15 pages, 662 KiB

Open AccessArticle

The Early Detection of Breast Cancer Using Liquid Biopsies: Model Estimates of the Benefits, Harms, and Costs

by Esmée K. J. van der Poort, Nicolien T. van Ravesteyn, Jeroen J. van den Broek and Harry J. de Koning

Cancers 2022, 14(12), 2951; https://doi.org/10.3390/cancers14122951 - 15 Jun 2022

Cited by 9 | Viewed by 2879

Abstract

Breast cancer screening is associated with harms, such as false-positives and overdiagnoses, and, thus, novel screen tests can be considered. Liquid biopsies have been proposed as a novel method for the early detection of cancer, but low cell-free DNA tumor fraction might pose a problem for the use in population screening. Using breast cancer microsimulation model MISCAN-Fadia, we estimated the outcomes of using liquid biopsies in breast cancer screening in women aged 50 to 74 in the United States. For varying combinations of test sensitivity and specificity, we quantify the impact of the use of liquid biopsies on the harms and benefits of screening, and we estimate the maximum liquid biopsy price for cost-effective implementation in breast cancer screening at a cost-effectiveness threshold of USD 50,000. We investigate under what conditions liquid biopsies could be a suitable alternative to digital mammography and compare these conditions to a CCGA substudy. Outcomes were compared to digital mammography screening, and include mortality reduction, overdiagnoses, quality-adjusted life-years (QALYs), and the maximum price of a liquid biopsy for cost-effective implementation. When liquid biopsies are unable to detect DCIS, a large proportion of overdiagnosed cases is prevented but overall breast cancer mortality reduction and quality of life are lower, and costs are higher compared to digital mammography screening. Liquid biopsies prices should be restricted to USD 187 per liquid biopsy depending on test performance. Overall, liquid biopsies that are unable to detect ductal carcinoma in situ (DCIS) need to be able to detect small, early-stage tumors, with high specificity, at low costs in order to be an alternative to digital mammography. Liquid biopsies might be more suitable as an addition to digital mammography than as an alternative. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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11 pages, 1080 KiB

Open AccessArticle

Extracellular Vesicle-Based Bronchoalveolar Lavage Fluid Liquid Biopsy for EGFR Mutation Testing in Advanced Non-Squamous NSCLC

by In Ae Kim, Jae Young Hur, Hee Joung Kim, Wan Seop Kim and Kye Young Lee

Cancers 2022, 14(11), 2744; https://doi.org/10.3390/cancers14112744 - 31 May 2022

Cited by 11 | Viewed by 2437

Abstract

To overcome the limitations of the tissue biopsy and plasma cfDNA liquid biopsy, we performed the EV-based BALF liquid biopsy of 224 newly diagnosed stage III-IV NSCLC patients and compared it with tissue genotyping and 110 plasma liquid biopsies. Isolation of EVs from BALF was performed by ultracentrifugation. EGFR genotyping was performed through peptide nucleic acid clamping-assisted fluorescence melting curve analysis. Compared with tissue-based genotyping, BALF liquid biopsy demonstrated a sensitivity, specificity, and concordance rates of 97.8%, 96.9%, and 97.7%, respectively. The performance of BALF liquid biopsy was almost identical to that of standard tissue-based genotyping. In contrast, plasma cfDNA-based liquid biopsy (n = 110) demonstrated sensitivity, specificity, and concordance rates of 48.5%, 86.3%, and 63.6%, respectively. The mean turn-around time of BALF liquid biopsy was significantly shorter (2.6 days) than that of tissue-based genotyping (13.9 days; p < 0.001). Therefore, the use of EV-based BALF shortens the time for confirmation of EGFR mutation status for starting EGFR-TKI treatment and can hence potentially improve clinical outcomes. As a result, we suggest that EV-based BALF EGFR testing in advanced lung NSCLC is a highly accurate rapid method and can be used as an alternative method for lung tissue biopsy. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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16 pages, 6787 KiB

Open AccessArticle

miRGalaxy: Galaxy-Based Framework for Interactive Analysis of microRNA and isomiR Sequencing Data

by Ilias Glogovitis, Galina Yahubyan, Thomas Würdinger, Danijela Koppers-Lalic and Vesselin Baev

Cancers 2021, 13(22), 5663; https://doi.org/10.3390/cancers13225663 - 12 Nov 2021

Cited by 5 | Viewed by 8668

Abstract

Tools for microRNA (miR) sequencing data analyses are broadly used in biomedical research. However, the complexity of computational approaches still remains a challenge for biologists with scarce experience in data analytics and bioinformatics. Here, we present miRGalaxy, a Galaxy-based framework for comprehensive analysis of miRs and their sequence variants—miR isoforms (isomiRs). Though isomiRs are commonly reported in deep-sequencing experiments, their detailed structure complexity and specific differential expression (DE) remain not fully examined by the majority of the available analysis tools. miRGalaxy encompasses biologist-user-friendly tools and workflows dedicated to the analysis of the isomiR-ome and its complex behavior in various biological samples. miRGalaxy is developed as a modular, accessible, redistributable, shareable, and user-friendly framework for scientists working with small RNA (sRNA)-seq data. Due to its modular workflow, advanced users can customize the steps and tools for their needs. In addition, the framework provides an analysis report where the significant output results are summarized in charts and visualizations. miRGalaxy can be accessed via preconfigured Docker image flavor and a Toolshed installation if the user already has a running Galaxy instance. Over the last decade, studies on the expression of miRs and isomiRs in normal and deregulated tissues have led to the discovery of their potential as diagnostic biomarkers. The detection of miRs in biofluids further expanded the exploration of the miR repertoire as a source of liquid biopsy biomarkers. Here we show the miRGalaxy framework application for in-depth analysis of the sRNA-seq data from two different biofluids, milk and plasma, to identify, annotate, and discover specific differentially expressed miRs and isomiRs. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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Review

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31 pages, 787 KiB

Open AccessReview

The Role of Cell-Free DNA in Cancer Treatment Decision Making

by András Telekes and Anna Horváth

Cancers 2022, 14(24), 6115; https://doi.org/10.3390/cancers14246115 - 12 Dec 2022

Cited by 16 | Viewed by 4006

Abstract

The aim of this review is to evaluate the present status of the use of cell-free DNA and its fraction of circulating tumor DNA (ctDNA) because this year July 2022, an ESMO guideline was published regarding the application of ctDNA in patient care. This review is for clinical oncologists to explain the concept, the terms used, the pros and cons of ctDNA; thus, the technical aspects of the different platforms are not reviewed in detail, but we try to help in navigating the current knowledge in liquid biopsy. Since the validated and adequately sensitive ctDNA assays have utility in identifying actionable mutations to direct targeted therapy, ctDNA may be used for this soon in routine clinical practice and in other different areas as well. The cfDNA fragments can be obtained by liquid biopsy and can be used for diagnosis, prognosis, and selecting among treatment options in cancer patients. A great proportion of cfDNA comes from normal cells of the body or from food uptake. Only a small part (<1%) of it is related to tumors, originating from primary tumors, metastatic sites, or circulating tumor cells (CTCs). Soon the data obtained from ctDNA may routinely be used for finding minimal residual disease, detecting relapse, and determining the sites of metastases. It might also be used for deciding appropriate therapy, and/or emerging resistance to the therapy and the data analysis of ctDNA may be combined with imaging or other markers. However, to achieve this goal, further clinical validations are inevitable. As a result, clinicians should be aware of the limitations of the assays. Of course, several open questions are still under research and because of it cfDNA and ctDNA testing are not part of routine care yet. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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14 pages, 714 KiB

Open AccessReview

The Practicality of the Use of Liquid Biopsy in Early Diagnosis and Treatment Monitoring of Oral Cancer in Resource-Limited Settings

by Henry Ademola Adeola, Ibrahim O. Bello, Raphael Taiwo Aruleba, Ngiambudulu M. Francisco, Tayo Alex Adekiya, Anthonio Oladele Adefuye, Paul Chukwudi Ikwegbue and Fungai Musaigwa

Cancers 2022, 14(5), 1139; https://doi.org/10.3390/cancers14051139 - 23 Feb 2022

Cited by 21 | Viewed by 4681

Abstract

An important driving force for precision and individualized medicine is the provision of tailor-made care for patients on an individual basis, in accordance with best evidence practice. Liquid biopsy(LB) has emerged as a critical tool for the early diagnosis of cancer and for treatment monitoring, but its clinical utility for oral squamous cell carcinoma (OSCC) requires more research and validation. Hence, in this review, we have discussed the current applications of LB and the practicality of its routine use in Africa; the potential advantages of LB over the conventional “gold-standard” of tissue biopsy; and finally, practical considerations were discussed in three parts: pre-analytic, analytic processing, and the statistical quality and postprocessing phases. Although it is imperative to establish clinically validated and standardized working guidelines for various aspects of LB sample collection, processing, and analysis for optimal and reliable use, manpower and technological infrastructures may also be an important factor to consider for the routine clinical application of LB for OSCC. LB is poised as a non-invasive precision tool for personalized oral cancer medicine, particularly for OSCC in Africa, when fully embraced. The promising application of different LB approaches using various downstream analyses such as released circulating tumor cells (CTCs), cell free DNA (cfDNA), microRNA (miRNA), messenger RNA (mRNA), and salivary exosomes were discussed. A better understanding of the diagnostic and therapeutic biomarkers of OSCC, using LB applications, would significantly reduce the cost, provide an opportunity for prompt detection and early treatment, and a method to adequately monitor the effectiveness of the therapy for OSCC, which typically presents with ominous prognosis. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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21 pages, 2854 KiB

Open AccessReview

Nipple Aspirate Fluid at a Glance

by Susana I. S. Patuleia, Karijn P. M. Suijkerbuijk, Elsken van der Wall, Paul J. van Diest and Cathy B. Moelans

Cancers 2022, 14(1), 159; https://doi.org/10.3390/cancers14010159 - 29 Dec 2021

Cited by 9 | Viewed by 3550

Abstract

Nipple aspirate fluid (NAF) is an intraductal mammary fluid that, because of its close proximity to and origin from the tissue from which breast cancer originates, is a promising source of biomarkers for early breast cancer detection. NAF can be non-invasively acquired via the nipple by aspiration using a suction device; using oxytocin nasal spray helps increase yield and tolerability. The aspiration procedure is generally experienced as more tolerable than the currently used breast imaging techniques mammography and breast magnetic resonance imaging. Future applications of NAF-derived biomarkers include their use as a tool in the detection of breast carcinogenesis at its earliest stage (before a tumor mass can be seen by imaging), or as a supporting diagnostic tool for imaging, such as when imaging is less reliable (to rule out false positives from imaging) or when imaging is not advisable (such as during pregnancy and breastfeeding). Ongoing clinical studies using NAF samples will likely shed light on NAF’s content and clinical potential. Here, we present a narrative review and perspectives of NAF research at a glance. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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Other

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11 pages, 1060 KiB

Open AccessSystematic Review

The Clinical Applications of Liquid Biopsies in Pediatric Brain Tumors: A Systematic Literature Review

by Ladina Greuter, Nicole Frank, Raphael Guzman and Jehuda Soleman

Cancers 2022, 14(11), 2683; https://doi.org/10.3390/cancers14112683 - 28 May 2022

Cited by 11 | Viewed by 2457

Abstract

Background: Pediatric brain tumors are the most common solid tumor in children. Traditionally, tumor diagnosis and molecular analysis were carried out on tumor tissue harvested either via biopsy or resection. However, liquid biopsy allows analysis of circulating tumor DNA in corporeal fluids such as cerebrospinal fluid or blood. Methods: We performed a systematic review in Pubmed and Embase regarding the role of liquid biopsy in pediatric brain tumors. Results: Nine studies with a total of 570 patients were included. The preferred corporeal fluid for analysis with a relatively high yield of ct-DNA was cerebrospinal fluid (CSF). For high-grade glioma, liquid biopsy can successfully characterize H3K27mutations and predict tumor progression before it is radiographically detected. Moreover, liquid biopsy has the potential to distinguish between pseudo-progression and actual progression. In medulloblastoma, ct-DNA in the CSF can be used as a surrogate marker of measurable residual disease and correlates with response to therapy and progression of the tumor up to three months before radiographic detection. Conclusion: Liquid biopsy is primarily useful in high-grade pediatric brain tumors such as diffuse midline glioma or medulloblastoma. Disease detection and monitoring is feasible for both tumor entities. More trials to standardize its use for pediatric brain tumors are necessary. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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13 pages, 1044 KiB

Open AccessSystematic Review

Cell Free Methylated Tumor DNA in Bronchial Lavage as an Additional Tool for Diagnosing Lung Cancer—A Systematic Review

by Sara Witting Christensen Wen, Jan Wen, Torben Frøstrup Hansen, Anders Jakobsen and Ole Hilberg

Cancers 2022, 14(9), 2254; https://doi.org/10.3390/cancers14092254 - 30 Apr 2022

Cited by 3 | Viewed by 2370

Abstract

This systematic review investigated circulating methylated tumor DNA in bronchial lavage fluid for diagnosing lung cancer. PROSPERO registration CRD42022309470. PubMed, Embase, Medline, and Web of Science were searched on 9 March 2022. Studies of adults with lung cancer or undergoing diagnostic workup for suspected lung cancer were included if they used bronchial lavage fluid, analyzed methylated circulating tumor DNA, and reported the diagnostic properties. Sensitivity, specificity, and lung cancer prevalence were summarized in forest plots. Risk of bias was assessed using the QUADAS-2 tool. A total of 25 studies were included. All were case-control studies, most studies used cell pellet for analysis by quantitative PCR. Diagnostic sensitivity ranged from 0% for a single gene to 97% for a four-gene panel. Specificity ranged from 8% for a single gene to 100%. The studies employing a gene panel decreased the specificity, and no gene panel had a perfect specificity of 100%. In conclusion, methylated circulating tumor DNA can be detected in bronchial lavage, and by employing a gene panel the sensitivity can be increased to clinically relevant levels. The available evidence regarding applicability in routine clinical practice is limited. Prospective, randomized clinical trials are needed to determine the further usefulness of this biomarker. Full article

(This article belongs to the Special Issue Liquid Biopsy: Current Status and Future Perspectives)

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