Liquid Biopsy is Instrumental for 3PM Dimensional Solutions in Cancer Management
Abstract
:1. Introduction
2. Liquid Biopsy Classification
3. Liquid Biopsy Analysis: Advanced Technologies Manifest New Horizons in Cancer Management
3.1. Real-Time PCR
3.2. Digital PCR
3.3. Next-Generation Sequencing
3.4. Proteomics Analyses of Liquid Biopsy
4. Blood Samples as Currently Most Frequently Used Liquid Biopsy in Cancer Diagnostics
4.1. Circulating Tumor DNA
4.2. Circulating Cell-Free miRNAs
4.3. Extracellular Vesicles in Liquid Biopsy
4.4. The Significance of CTCs in Blood-Based Liquid Biopsy for Cancer Management
4.5. Other Biomarkers of Blood-Based Liquid Biopsy or Their Combinations
5. Other Liquid Biopsy Types
5.1. Urine-Based Liquid Biopsy
5.2. Salivary Liquid Biopsy
5.3. Cerebrospinal Fluid-Based Liquid Biopsy
5.4. Liquid Biopsy Based on Other Bio-Fluids
6. Liquid Biopsy as a Tool for Screening and Early Cancer Diagnosis
7. Concluding Remarks and 3PM-Related Expert Recommendations
Author Contributions
Funding
Conflicts of Interest
References
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Technology | Cancer Type | Liquid Biopsy Type | Biomarker | Reference |
---|---|---|---|---|
RT-PCR | CRC | Plasma | ↑ Methylation of SEPT9 | [48] |
CRC | Plasma | ↓ miR-145, -195 ↑ miR-29, 92 | [49] | |
Gastric cancer | Plasma | ↓ miR-195-5p | [50] | |
Glioblastoma | CSF | ↑ miR-21 | [51] | |
CNS malignancies | CSF | Differently expressed miR-771, -451, -223, -935, -125b | [52] | |
UCC | Urine | gene expression signatures for UCC | [53] | |
Bladder cancer | Urine | ↓ miR-145, -200 | [54] | |
Bladder cancer | Urine | ↑ UBE2C | [55] | |
OSCC | Saliva | ↓ miR-125, -200a | [56] | |
EC | Saliva | ↑ miR-10b, -21, -144 and -451 | [57] | |
EC | Saliva | ↑ miR-21 | [58] | |
Lung adenocarcinoma | PE | ↑ miR-195-5p, -182-5p, and -34a-5p | ||
dPCR | HNSCC | Plasma | Detection of TP53 mutation | [61] |
Melanoma | Plasma | Detection of BRAFV600E mutation | [62] | |
Metastatic adenocarcinoma | Plasma | Detection of KRAS mutation | [63] | |
Central nervous system lymphomas | CSF | Detection of MYD88 p.(L265P) | [64] | |
Glioma | CSF | Analysis of mutant IDH1 mRNA | [67] | |
Bladder cancer | Urine | Identification of TERT mutation | [65] | |
NSCLC | Urine | Identification of EGFR mutation | [66] | |
NSCLC | PE | Identification of EGFR mutation | [70] | |
NGS | NSCLC | Plasma | Detection of oncogenic drivers and resistance mechanisms | [74] |
EC | Plasma | Detection of somatic mutations associated with recurrence of disease | [83] | |
LAC with LM | CSF | Detection of tumor associated mutations | [75] | |
NSCLC with LM | CSF | Detection of targetable changes | [76] | |
LC | PE | Identification of alterations in tumor genomics | [77] | |
MS | Multiple myeloma | Urine | Identification of urine biomarker | [80] |
Liver cancer | Serum | Analysis of total serum protein fingerprints | [81] | |
ESCC | Plasma | Identification of plasma biomarkers | [82] |
Biomarker | Cancer Type | Study Characteristic (Number of Patients) | Study Results | Reference |
---|---|---|---|---|
Circulating tumor DNA | ||||
ctDNA (serum) | NSCLC | NSCLC patients (n = 60), COPD patients (n = 40) and healthy controls (n = 40) | Discrimination of normal individuals from COPD and NSCLC. ctDNA high level → short survival of NSCLC patients. | [86] |
ctDNA (serum) | Advanced NSCLC | Patients rechallenged with gefitinib at progression after second-line chemotherapy (n = 61) | An identification of EGFR-mutant patients: those not carrying p.T790M variant with no other alternative treatment might benefit from TKI rechallenge. | [87] |
Formalin-fixed, paraffin-embedded, metastatic tissue and corresponding ctDNA (serum) | Advanced breast cancer | Metastatic breast cancer patients (n = 66) | PIK3CA mutation tumor tissue and detectable PIK3CA mutations in serum ctDNA in 83% of cases. Correlation between changes in PIK3CA ctDNA level and treatment response. | [106] |
HPV-specific E7 and L1 genes (ctDNA, plasma) | Cervical cancer | Cervical cancer patients (n = 138) | HPV E7 and L1 sequences detected in plasma ctDNA (61.6% of patients). High viral load: increased risk of recurrence and death at 5 years (univariate analysis). | [107] |
Combined exosomal RNA and ctDNA (plasma) | NSCLC | Mutant EGFR NSCLC patients (n = 84) | Increased sensitivity for EGFR mutation detection, especially in patients with intrathoracic metastatic disease (low levels of ctDNA). | [108] |
Methylation level in circulating cell-free DNA (serum, plasma) | Breast cancer | Serum test cohort (n = 103), serum validation cohort (n = 368), and plasma cohort (n = 125) | Serum test cohort: panel of SPAG6 and ITIH5 → 63% sensitivity of DCIS and 51% sensitivity for early invasive tumor detection at 80% specificity. The serum validation cohort: 50% sensitivity for DCIS detection (NKX2-6 and ITIH5). | [112] |
Methylation level in circulating cell-free DNA (plasma) | Lung cancer | Tissue samples (n = 152), plasma samples (n = 129), and benign lesions of lung (n = 28) | Plasma samples: higher methylation of HOXA9 and RASSF1A in SCLC than in NSCLC. | [89] |
Cell-free DNA sequencing informative methylation patterns (plasma) | More than 50 cancer types | Participants with (n = 8584) and without (n = 6670) cancer | Detection of more than 50 cancer types across stages. | [113] |
Circulating miRNAs in liquid biopsy | ||||
miRNA (serum) | Lung cancer | Preliminary marker selection (early-stage lung cancer n = 24 and healthy control n =24) and a validation phase (early-stage lung cancer n = 94, stage II to IV n = 48, and healthy control n = 111) | Potential of combination of miR-125a-5p, miR-25, and miR-126 in early detection of lung cancer. | [118] |
miRNA (serum) | Prostate cancer | Prostate cancer patients (n = 809), negative prostate biopsies (n = 241), patients with other cancer types (n = 500), and healthy controls (n = 41) | Potential of combination of miR-17-3p and miR-1185-2-3p as a marker of prostate cancer diagnosis. | [119] |
miRNA (serum) | Bladder cancer | Bladder cancer patients (n = 392), non-cancer samples (n = 100), and other cancer types (n = 480) | Set of 7 miRNAs (miR-6087, miR-1185-1-3p, miR-3960, miR-6724-5p, miR-1343-5p, miR-6831-5p and miR-4695-5p): discrimination of bladder cancer from non-cancer and other types of cancer. | [120] |
miRNA (serum) | Breast, endometrial and ovarian cancer | Breast cancer (n = 31), endometrial cancer (n = 13), and ovarian cancer (n = 15) patients | miR-518b, -4719 and -6757-3p deregulated in breast cancer. miR-484/-23a diagnostic biomarker for endometrial and ovarian cancer. | [121] |
Extracellular vesicles in liquid biopsy | ||||
Circulating exosomes (serum) | ESCC | ESCC patients (n = 200) | Upregulated level of circulating exosomes in ESCC patients. | [91] |
Circulating exosomal DNA (serum) | PDAC | PDAC patients (n = 48) and healthy subjects (n = 114) | Highlighting the role of circulating exosomal DNA in rapid identification of cancer driving mutations. | [92] |
EV-miRNAs (serum) | mCRC | mCRC (n = 44) and healthy controls (n = 17) | Baseline miRNA-21 and -92a outperformed carcinoembryonic antigen levels in mCRC patients when compared to healthy controls. Higher levels of miRNA-92a and 222 in patients who died. | [93] |
Circulating tumor cells | ||||
CTCs | Prostate cancer patients | Prostate cancer patients with CTCs <5 (n = 511) | Increasing CTCs associated with worse overall survival of patients treated with chemotherapy of endocrine therapy. | [137] |
Metastatic breast cancer patients | Metastatic breast cancer patients receiving eribulin treatment (n = 21) | Determination of mesenchymal and epithelial CTCs for the prediction of survival. | ||
SCLC | SCLC patients before pazopanib initiation (n = 56 patients), after one-cycle (n = 35), and on disease progression (n = 45) | Analysis of CTCs as biomarkers of treatment efficacy (pazopanib eliminates CTC subpopulations). | [139] | |
EOC | EOC patients (n = 109) | Detection of CTCs and their pattern of gene expression could predict the likelihood of chemotherapy resistance and evaluate the prognosis of ovarian cancer patients. | [140] | |
NSCLC | Advanced-stage NSCLC patients (n = 45) | Identification of CTCs through EGFR/HER3 expression →novel liquid biopsy approach. | [141] | |
EOC | EOC patients (n = 10) | The feasibility and potential usefulness of chemosensitivity assay using liquid biopsy-derived CTCs in the prediction of response to therapy. | [142] | |
Ewing sarcoma | Ewing sarcoma patients (n = 18) and healthy volunteers (n = 9) | Identification of CTCs by immunoseparation with CD99 antibody and magnetic microbeads → prognostic and predictive potential. | [143] | |
CRC (draining venous blood) | CRC patients (n = 26) and healthy volunteers (n = 14) | New filtration and cytology-based automated platform for detection of CTCs → prognostic and predictive potential. | [144] | |
Other biomarkers of blood-based liquid biopsy or their combinations | ||||
Soluble PD-L1 and PD-L2 (serum) | EOC | EOC patients (n = 83) and healthy controls (n = 29) | Soluble PD-L1 increased and PD-L2 decreased in EOC. Enhanced soluble PD-L1: residual tumor burden and reduced 5 year overall survival and progression-free survival. Reduced soluble PD-L2: platinum-resistance. | [145] |
sCRT | Ovarian cancer | Ovarian cancer patients (n = 134) and healthy controls (n = 116) | Increased sCRT in ovarian cancer patients. sCRT predictor of poor prognosis and platinum resistance. | [94] |
sGKN1 | Gastric cancer | Advanced gastric cancer patients (n = 360), early gastric cancer patients (n = 140), and healthy controls (n = 200) | Increased sGKN1 in healthy subjects when compared with gastric cancer patients. Decreased sGKN1 in advanced gastric cancer when compared with early gastric cancer. | [95] |
Serum proteins and miRNAs | Cervical cancer | Early-stage cervical cancer patients (n = 140) and healthy controls (n = 140). Independent cohort study (early-stage cervical cancer patients n = 60 and healthy controls n = 60) | Combination of SCC Ag degree and miRNA-29a, miRNA-25, and miRNA-486-5p levels as a marker of early-stage cervical cancer detection. | [98] |
miRNA and fecal hemoglobin concentration (serum) | Colorectal carcinoma | CRC patients (n = 59), advanced adenomas (n = 74) and control subjects (n = 80) | Potential of a combination of 6 miRNAs (miR-15b-5p, miR-29a-3p, miR-335-5p, miR-18a-5p, miR-19a-3p and miR-19b-3p) and fecal hemoglobin concentration in the detection of advanced colorectal cancer in average risk individuals. | [146] |
Histone modifications (serum) | Hepatocellular carcinoma | Hepatocellular carcinoma patients’ blood samples (n = 24) and healthy volunteers (n = 6) | Serum purified histones: comparable pattern of modifications like acetylation (H4K16Ac), methylation (H4K20Me3, H3K27Me3, H3K9Me3) and phosphorylation (γ-H2AX and H3S10P) to paired cancer tissues. | [96] |
Histone modifications (plasma) | CRC | CRC patients (n = 63) and control subjects (n = 40) | Lower H3K27me3 and H4K20me3 in CRC patients when compared to healthy control. | [97] |
Biomarker | Cancer Type | Study Characteristics | Study Results | Reference |
---|---|---|---|---|
Tumor DNA (urine supernatant) | NMIBC | NMIBC patients (n = 216) and patients with bladder cancer undergoing radical cystectomy (n = 27) | An association between high levels of tumor DNA and later disease progression in NMIBC. | [158] |
6-gene (APC2, CDH1, FOXP1, LRRC3B, WNT7A and ZIC4) promoter methylation (urine cell-free DNA) | Prostate cancer | Prostate cancer patients (n = 31) and control subjects (n = 33) | NGM increased monotonically from 0.27 in control subjects to 4.6 and 4.25 in patients with highly developed and T2/T3 stage metastatic prostate cancer, respectively. | [159] |
ctDNA (plasma, urine) | mCRC | mCRC patients (n = 150) | Utilization of both plasma and urine cell-free DNA to address disease progression in CRC patients. | [160] |
EGFR and TP53 mutations (plasma, urine, sputum) | NSCLC | NSCLC patients (n = 50) | Increase in the detection of EGFR or TP53 mutation with higher sensitivity by a combination of plasma, sputum and urine. | [161] |
Lipids in urinary exosomes | Prostate cancer | Prostate cancer patients (n = 15) and healthy controls (n = 13) | Different levels of lipid species in the two groups. | [24] |
miRNA | ccRCC | ccRCC patients (n = 75) and control subjects (n = 45) | Higher urinary cell-free miRNA-210 in ccRCC vs. control. Decreased urinary cell-free miRNA-210 in ccRCC patients a week after surgery. | [163] |
miRNA (urine-derived exosomes) | Endometrial cancer | Endometrial cancer patients (n = 22) and symptomatic controls (n = 5) | The potential utilization of differential miRNA in exosomes as biomarker in diagnosis of endometrial cancer (hsa-miR-200c-3p as a candidate). | [165] |
miRNAs | Bladder cancer | Identification of miRNA fingerprints: bladder cancer patients (n = 66) and control subjects (n = 48). Altered miRNAs validation: bladder cancer patients (n = 112) and control subjects (n = 65) | AUC (miR-30a-5p, let-7c-5p, miR-486-5p) altered in all bladder cancer subtypes → increased accuracy in the discrimination of cases and controls. | [164] |
Biomarker | Cancer Type | Study Characteristics | Study Results | Reference |
---|---|---|---|---|
mRNA (saliva) and blood CTCs | NSCLC | Discovery phase: NSCLC patients (n = 140) and healthy controls (n = 140). Validation phase: NSCLC patients (n = 60) and healthy controls (n = 60). | Panel of CTC level in blood and mRNA markers in saliva (CCNI, EGFR, FGF19, FRS2, GREB1): discrimination of NSCLC from healthy controls. | [15] |
mRNA (saliva) and CEA (blood) | NSCLC | Discovery phase: NSCLC patients (n = 30) and healthy controls (n = 30). Prediction performance evaluation: NSCLC patients (n = 15) and healthy controls (n = 25). | Panel measuring CEA in blood and GREB1 and FRS2 levels in saliva could be used for the detection of NSCLC. | [170] |
miRNAs (saliva) | CRC | Discovery phase (healthy controls n = 10 and CRC patients n = 14) and validation phase (healthy controls n = 37, CRC patients n = 51, and adenoma n = 19) | Panel of saliva-based miRNAs (miR-186-5p, miR-29a-3p, miR-29c-3p, miR-766-3p, and miR-491-5p) higher in CRC vs. control → detection of CRC. | [11] |
miRNAs (salivary exosomes) | Pancreatobiliary tract cancer | Pancreatobiliary tract cancer (n = 12) and healthy controls (n = 13) | Relative expression ratios of miR-1246 and miR-4644 significantly higher in cancer group vs. control. The potential of miR-1246 and miR-4644 in salivary exosomes as candidate biomarkers. | [173] |
Proteins (salivary exosomes) | Lung cancer | Lung cancer patients and normal subjects | The potential use of informative proteins in salivary EVs for detection of lung cancer. | [174] |
Salivary exosomes | Isolation of salivary exosomes by the acoustofluidic (the fusion of acoustics and microfluidics) platform → potential in the detection of HPV-OPC. | [176] | ||
ctDNA containing EGFR mutations (saliva, plasma) | Electric field-induced release and measurement → novel platform detecting ctDNA containing EGFR mutations directly from plasma and saliva in early- and late-stage NSCLC. | [177] |
Biomarker | Cancer Type | Study Characteristics | Study Results | Reference |
---|---|---|---|---|
CSF metabolites | Primary or metastatic central nervous system tumors | Patients without a history of cancer (n = 8) and with a variety of CNS tumor types (n = 23) (i.e., glioma IDH mutant, glioma IDH wildtype, metastatic lung cancer and metastatic breast cancer) | Differences in the abundance of 43 metabolites between CSF from control patients and the CSF of patients with primary or metastatic CNS tumors. Alterations in metabolic pathways (e.g., glycine, choline and methionine degradation, diphthamide biosynthesis and glycolysis pathways, among others) between IDH-mutant and IDH-wildtype gliomas. IDH-mutant gliomas: higher levels of D-2-hydroxyglutarate in CSF in comparison to patients with other tumor types or controls. | [25] |
ctDNA (CSF, plasma) | HER2-positive breast cancer with brain metastases | CSF-derived ctDNA analysis: TP53, PIK3CA mutations and ERBB2 and cMYC amplification. Post-treatment ctDNA analysis: decreased marker levels in plasma (consistent with extra-CNS disease control) and increased CSF (poor treatment benefit in the CNS). | [181] | |
ctDNA (blood, CSF) | NSCLC with brain metastasis | NSCLC patients with brain metastasis (n = 21) | Specific genetic mutation patterns in driver genes: EGFR mutations: 57.1% (in CSF ctDNA) and 23.8% (in peripheral blood ctDNA and in CTCs). EGFR mutations found in CSF of 81.8% patients with leptomeningeal metastases and 30% patients with brain parenchymal metastases. The status of EGFR and TP53 mutations was consistent between CSF ctDNA and brain lesion tissue in all five patients. | [182] |
Biomarker | Cancer Type | Study Characteristics | Study Results | Reference |
---|---|---|---|---|
Ascites-based liquid biopsy | ||||
Malignant ascites | Gastrointestinal cancer | Patients diagnosed with malignant ascites of gastrointestinal cancer (n = 27) | Large amount of CD4+ and CD8+ T cells: exhausted phenotype → significant clinical relevance as prognostic and therapeutic target. | [30] |
Pleural effusion | ||||
EGFR (pleural effusion, ascites, pericardial effusion and cerebrospinal fluid) | Lung adenocarcinoma patients | Lung adenocarcinoma patients (n = 20) | Higher detection rate sensitivity of tumor-specific EGFR mutations in biofluid-supernatant-free DNA in comparison with biofluid sediment tumor cells and plasma-free DNA samples. | [187] |
Bronchoalveolar lavage | ||||
EGFR (bronchoalveolar lavage fluid, EVs) | NSCLC | NSCLC patients (n = 137) | EGFR genotyping by bronchoalveolar lavage fluid obtained from tumor site: high accuracy of diagnosis. | [153] |
TMPRSS4 methylation (bronchoalveolar lavage and plasma) | NSCLC | Bronchoalveolar lavage: lung cancer patients (n = 79) and healthy controls (n = 26). Plasma: lung cancer patients (n = 89) and healthy controls (n = 25). | Monitoring of surgically resected NSCLC patients. TMPRSS4 methylation status differentiates NSCLC and tumor-free subjects. | [188] |
Peritoneal lavage | ||||
EV-isolated miRNAs (peritoneal lavage, ascites) | CRC | CRC patients (n = 25) and control patients (n = 25) | Source of potential biomarkers for CRC diagnosis (miRNA-199b-5p, miRNA-150-5p, miRNA-29c-5p, miRNA-218-5p, miRNA-99a-3p, miRNA-383-5p, miRNA-199a-3p, miRNA-193a-5p, miRNA-10b-5p and miRNA-181c-5p). | [38] |
EV-isolated miRNAs (peritoneal lavage, ascites) | Endometrial cancer | Endometrial cancer patients (n = 25) and control patients (n = 25) | Deregulated miRNAs in endometrial cancer (n = 114) miRNAs. miRNA-383-5p, miRNA-10b-5p, miRNA-34c-3p, miRNA-449b-5p, miRNA-34c-5p, miRNA-200b-3p, miRNA-2110, and miRNA-34b-3p highlighted as promising biomarkers. | [190] |
KRAS and PIK3CA mutational analysis (peritoneal lavage, blood) | Endometrial cancer | Endometrial cancer patients (n = 50) | Approved feasibility of mutational analysis. Further studies needed to determine its use in the identification of patients with worse prognosis. | [191] |
Uterine/utero-tubular lavage | ||||
PTEN mutations (uterine lavage fluid) | Endometrial cancer | 67-year-old asymptomatic female | Identification of two oncogenic PTEN mutations nearly one year before the occurrence of symptoms | [192] |
Genomic profiling (uterine aspirate, blood) | Endometrial cancer | Endometrial cancer patients (n = 60) | Potential applicability of combined use of different liquid biopsy for personalized cancer management. | [10] |
Microvesicle proteomic profiling (utero-tubal lavage) | Ovarian cancer | High-grade ovarian cancer patients (n = 49) and controls (n = 127) | 9-protein classifier with 70% sensitivity and 76.2% specificity (identified all stage I lesions). | [35] |
Cervical and vaginal secretions | ||||
CA-125 (cervical and vaginal secretions, serum) | Endometrial cancer | Patients with polyps, hyperplasia or endometrial cancer (n = 97) and healthy subjects (n = 51) | Increased CA-125 in patients with complex hyperplasia and endometrial cancer. | [193] |
Tear fluid | ||||
Proteomic pattern | Breast cancer | Primary invasive breast carcinoma patients (n = 25) and healthy controls (n = 25) | Identified diagnostic protein biomarker to differentiate cancer patients from controls. | [150,194] |
Breast cancer patients (n = 50) and healthy controls (n = 50) | ||||
Tear exosomes (miRNAs) | Breast cancer | Metastatic breast cancer patients (n = 5) and healthy controls (n = 8) | Higher quantity of exosome markers in tears than in serum. Highly expressed miRNA-21 and miRNA-200c in tear exosomes of metastatic breast cancer patients in comparison with controls. | [195] |
Breast milk | ||||
Proteins | Breast cancer | Ten milk samples from eight females | Identification of protein for early detection and accurate assessment of breast cancer. | [151] |
Breast ductal fluid | ||||
miRNAs | Unilateral breast cancer | Unilateral breast cancer patients (n = 22) | Feasibility of analyzing miRNAs. Discrimination of tumor histological subtypes. Discrimination of cancer and normal breast samples. | [154] |
Seminal fluid | ||||
ctDNA (seminal plasma) | Prostate cancer | Prostate cancer patients (n = 6) and healthy controls (n = 3) | Different concentrations and fragment size of seminal plasma ctDNA in prostate cancer patients, benign prostate hyperplasia and healthy controls. | [33,152] |
Prostate cancer patients (n = 30), benign prostate hyperplasia patients (n = 33), and healthy controls (n = 21) |
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Liskova, A.; Samec, M.; Koklesova, L.; Giordano, F.A.; Kubatka, P.; Golubnitschaja, O. Liquid Biopsy is Instrumental for 3PM Dimensional Solutions in Cancer Management. J. Clin. Med. 2020, 9, 2749. https://doi.org/10.3390/jcm9092749
Liskova A, Samec M, Koklesova L, Giordano FA, Kubatka P, Golubnitschaja O. Liquid Biopsy is Instrumental for 3PM Dimensional Solutions in Cancer Management. Journal of Clinical Medicine. 2020; 9(9):2749. https://doi.org/10.3390/jcm9092749
Chicago/Turabian StyleLiskova, Alena, Marek Samec, Lenka Koklesova, Frank A. Giordano, Peter Kubatka, and Olga Golubnitschaja. 2020. "Liquid Biopsy is Instrumental for 3PM Dimensional Solutions in Cancer Management" Journal of Clinical Medicine 9, no. 9: 2749. https://doi.org/10.3390/jcm9092749