Extraction of Cell-Free DNA

Abstract

Cell-free DNA (cfDNA) serves as a valuable biomarker for early disease detection and monitoring. However, the use of cfDNA for analysis faces challenges owing to general low but variable abundance and fragmentation. Preanalytical factors, including cfDNA extraction, impact cfDNA quality and quantity. Efficient and robust cfDNA extraction is essential for reliable results in downstream applications, and various commercial extraction methods exist, each with trade-offs. To aid researchers and clinicians in choosing the proper cfDNA extraction method, manual, semiautomated, and automated methods were evaluated, including the QIAamp Circulating Nucleic Acid Kit (manual and QIAcube), QIAamp MinElute ccfDNA Kit (QIAcube), and QIAsymphony DSP Circulating DNA Kit (QIAsymphony). For each extraction method, cfDNA was extracted on two separate days, using samples obtained from 18 healthy donors. This study assessed extraction efficiency, quantity, and quality using droplet digital PCR and TapeStation. The QIAamp Circulating Nucleic Acid Kit, both manual and semiautomated, outperformed the QIAamp MinElute ccfDNA Kit (QIAcube) and QIAsymphony DSP Circulating DNA Kit (QIAsymphony), showing higher recovery rates and cfDNA quantity. All methods were reproducible, with no day-to-day variability and no contamination by high-molecular-weight DNA. The QIAamp Circulating Nucleic Acid Kit offers high yield without compromising quality. Implementation of the method should consider specific study and clinical needs, taking into account each method's advantages and limitations for optimal outcomes. Cell-free DNA (cfDNA) serves as a valuable biomarker for early disease detection and monitoring. However, the use of cfDNA for analysis faces challenges owing to general low but variable abundance and fragmentation. Preanalytical factors, including cfDNA extraction, impact cfDNA quality and quantity. Efficient and robust cfDNA extraction is essential for reliable results in downstream applications, and various commercial extraction methods exist, each with trade-offs. To aid researchers and clinicians in choosing the proper cfDNA extraction method, manual, semiautomated, and automated methods were evaluated, including the QIAamp Circulating Nucleic Acid Kit (manual and QIAcube), QIAamp MinElute ccfDNA Kit (QIAcube), and QIAsymphony DSP Circulating DNA Kit (QIAsymphony). For each extraction method, cfDNA was extracted on two separate days, using samples obtained from 18 healthy donors. This study assessed extraction efficiency, quantity, and quality using droplet digital PCR and TapeStation. The QIAamp Circulating Nucleic Acid Kit, both manual and semiautomated, outperformed the QIAamp MinElute ccfDNA Kit (QIAcube) and QIAsymphony DSP Circulating DNA Kit (QIAsymphony), showing higher recovery rates and cfDNA quantity. All methods were reproducible, with no day-to-day variability and no contamination by high-molecular-weight DNA. The QIAamp Circulating Nucleic Acid Kit offers high yield without compromising quality. Implementation of the method should consider specific study and clinical needs, taking into account each method's advantages and limitations for optimal outcomes. Cell-free DNA (cfDNA) is a valuable biomarker for early detection, identification, and monitoring of various diseases. As a minimally invasive technique, liquid biopsy has gained attention as an alternative to tissue biopsy, overcoming limitations such as sampling bias and tissue heterogeneity.1Marrugo-Ramírez J. Mir M. Samitier J. Blood-based cancer biomarkers in liquid biopsy: a promising non-invasive alternative to tissue biopsy.Int J Mol Sci. 2018; 19: 2877Crossref PubMed Scopus (259) Google Scholar,2Chu D. Park B.H. Liquid biopsy: unlocking the potentials of cell-free DNA.Virchows Arch. 2017; 471: 147-154Crossref PubMed Scopus (31) Google Scholar However, the analysis of cfDNA presents significant challenges because of its relatively low and variable abundance and high degree of fragmentation.3Perkins G. Yap T.A. Pope L. Cassidy A.M. Dukes J.P. Riisnaes R. Massard C. Cassier P.A. Miranda S. Clark J. Denholm K.A. Thway K. Gonzalez De Castro D. Attard G. Molife L.R. Kaye S.B. Banerji U. de Bono J.S. Multi-purpose utility of circulating plasma DNA testing in patients with advanced cancers.PLoS One. 2012; 7e47020Crossref Scopus (134) Google Scholar,4Fleischhacker M. Schmidt B. Circulating nucleic acids (CNAs) and cancer--a survey.Biochim Biophys Acta. 2007; 1775: 181-232Crossref PubMed Scopus (752) Google Scholar The quality and quantity of cfDNA are influenced by preanalytical factors, including the choice of sample material (plasma or serum), sample collection tubes, centrifugation regimen, storage conditions, cfDNA extraction methods, quantification methods, and downstream analysis.5Markus H. Contente-Cuomo T. Farooq M. Liang W.S. Borad M.J. Sivakumar S. Gollins S. Tran N.L. Dhruv H.D. Berens M.E. Bryce A. Sekulic A. Ribas A. Trent J.M. LoRusso P.M. Murtaza M. Evaluation of pre-analytical factors affecting plasma DNA analysis.Sci Rep. 2018; 8: 7375Crossref PubMed Scopus (96) Google Scholar, 6Bronkhorst A.J. Aucamp J. Pretorius P.J. Cell-free DNA: preanalytical variables.Clin Chim Acta. 2015; 450: 243-253Crossref PubMed Scopus (123) Google Scholar, 7Heitzer E. van den Broek D. Denis M.G. Hofman P. Hubank M. Mouliere F. Paz-Ares L. Schuuring E. Sültmann H. Vainer G. Verstraaten E. de Visser L. Cortinovis D. Recommendations for a practical implementation of circulating tumor DNA mutation testing in metastatic non-small-cell lung cancer.ESMO Open. 2022; 7100399Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar, 8Kang Q. Henry N.L. Paoletti C. Jiang H. Vats P. Chinnaiyan A.M. Hayes D.F. Merajver S.D. Rae J.M. Tewari M. Comparative analysis of circulating tumor DNA stability in K3EDTA, Streck, and CellSave blood collection tubes.Clin Biochem. 2016; 49: 1354-1360Crossref PubMed Scopus (161) Google Scholar, 9Meddeb R. Pisareva E. Thierry A.R. Guidelines for the preanalytical conditions for analyzing circulating cell-free DNA.Clin Chem. 2019; 65: 623-633Crossref PubMed Scopus (129) Google Scholar Efficient cfDNA extraction methods should be fast, robust, simple, and preferably automatable, ensuring satisfactory quality and yield of cfDNA for reliable results in downstream applications such as next-generation sequencing or digital PCR.10Phallen J. Sausen M. Adleff V. Leal A. Hruban C. White J. et al.Direct detection of early-stage cancers using circulating tumor DNA.Sci Transl Med. 2017; 9eaan2415Crossref PubMed Scopus (724) Google Scholar,11Underhill H.R. Kitzman J.O. Hellwig S. Welker N.C. Daza R. Baker D.N. Gligorich K.M. Rostomily R.C. Bronner M.P. Shendure J. Fragment length of circulating tumor DNA.PLoS Genet. 2016; 12e1006162Crossref PubMed Scopus (454) Google Scholar Various cfDNA extraction methods with different binding chemistries are available commercially.12Deans Z.C. Butler R. Cheetham M. Dequeker E.M.C. Fairley J.A. Fenizia F. Hall J.A. Keppens C. Normanno N. Schuuring E. Patton S.J. IQN path ASBL report from the first European cfDNA consensus meeting: expert opinion on the minimal requirements for clinical ctDNA testing.Virchows Arch. 2019; 474: 681-689Crossref PubMed Scopus (27) Google Scholar These include ethanol precipitation, anion-exchange resin, silica gel membrane binding, and magnetic silica particle binding technologies. Magnetic particle–based methods have advantages in terms of cost, speed, scalability, and automation, whereas membrane binding methods can yield higher amounts of cfDNA.13Xue X. Teare M.D. Holen I. Zhu Y.M. Woll P.J. Optimizing the yield and utility of circulating cell-free DNA from plasma and serum.Clin Chim Acta. 2009; 404: 100-104Crossref PubMed Scopus (125) Google Scholar The choice of method depends on the desired output, purity requirements, and downstream applications. To ensure optimal implementation of cfDNA analyses, assessing and evaluating the extraction efficiency, quality, and reproducibility of various cfDNA extraction methods is crucial. This evaluation helps in selecting the most appropriate methods that align with the specific requirements of the application. Therefore, a thorough comparative evaluation was performed using plasma samples obtained from healthy donors. This study assessed one manual cfDNA extraction method, two semiautomated methods, and one fully automated cfDNA extraction method. The evaluation focused on assessing the extraction efficiency, the quality of the extracted cfDNA, and the feasibility of the methods used. The findings provide valuable insights for researchers and clinicians in selecting the most suitable cfDNA extraction approach based on the specific requirements of their research and clinical applications. Blood samples were collected from 18 healthy donors at the Aalborg University Hospital Blood Bank (Aalborg, Denmark). Blood was drawn from each donor in four 9-mL EDTA blood collection tubes, and plasma was separated within 2 hours of blood draw using double centrifugation at 2000 × g for 10 minutes at 4°C. After each centrifugation, plasma was collected 5 mm above the buffy coat/pellet to avoid contamination from lymphocytes. All separated plasma from the four blood collection tubes was pooled. To evaluate the extraction efficiency, 5800 copies/mL of the 191 bp internal exogenous control glycine max mRNA for cysteine-rich polycomb-like protein (CPP1) (gBlock Gene Fragments; Integrated DNA Technologies, Inc., Coralville, IA)14Pallisgaard N. Spindler K.L.G. Andersen R.F. Brandslund I. Jakobsen A. Controls to validate plasma samples for cell free DNA quantification.Clin Chim Acta. 2015; 446: 141-146Crossref PubMed Scopus (57) Google Scholar was added to each plasma pool before the plasma was divided into 1-mL portions for subsequent processing. The CPP1 synthetic DNA fragment a from the protein CPP1 and is to to cfDNA cfDNA N. Spindler K.L.G. Andersen R.F. Brandslund I. Jakobsen A. Controls to validate plasma samples for cell free DNA quantification.Clin Chim Acta. 2015; 446: 141-146Crossref PubMed Scopus (57) Google Scholar All plasma samples were at cfDNA cfDNA was from plasma using the QIAamp Circulating Nucleic Acid Kit using the manual and the QIAamp MinElute ccfDNA Kit using the and QIAsymphony DSP Circulating DNA Kit using the QIAsymphony For cfDNA extraction methods, the cfDNA extraction was performed by one the For the QIAsymphony DSP Circulating DNA Kit, was added to the plasma samples to the for the For methods, the was to To the day-to-day variability to the extraction plasma samples from each donor were extracted on two for each method. cfDNA was at analysis in DNA tubes or in the collection tubes with the of cfDNA Kit and extraction Circulating Nucleic Acid or semiautomated using DSP Circulating DNA automated using on the of MinElute ccfDNA and using cell-free on the of in a cfDNA, cell-free DNA. To evaluate the extraction of cfDNA, the of CPP1 from the was with the of CPP1 cfDNA extraction using droplet digital PCR The recovery was as extraction of was of cfDNA was performed using with two in and membrane protein are by T. R. H. S. I. P. K. S. S. N. J.S. Andersen of circulating DNA to disease cancer 2016; 65: PubMed Scopus Google T. T. K. A. K. T. of in by droplet digital PCR in patients with 2019; PubMed Scopus Google Scholar quality to evaluating cfDNA extraction are contamination with high-molecular-weight DNA from and DNA fragmentation. The DNA contamination was assessed using the blood cell the of N. Spindler K.L.G. Andersen R.F. Brandslund I. Jakobsen A. Controls to validate plasma samples for cell free DNA quantification.Clin Chim Acta. 2015; 446: 141-146Crossref PubMed Scopus (57) Google Scholar was minimal contamination of DNA from whereas a was high The DNA fragment and of cfDNA were with using the Cell-free DNA on and Technologies, Inc., cfDNA as and the of to as of contamination of DNA was with as by et N. C. Spindler K.L.G. The clinical of circulating DNA in cell of the Scopus Google Scholar using two a fragment and a fragment of the was a low of DNA in the whereas a was DNA cfDNA extraction, is a of the to such as next-generation sequencing on the DNA to be in a a of the extracted DNA is the of DNA using is Therefore, assessing the of DNA and DNA for each cfDNA extraction method is To evaluate the of cfDNA for and cfDNA were of two a of in the using were using a cfDNA quality control of and 10 was performed to the and with each of of each of each and 5 DNA. were using the The PCR was performed on a with the PCR for 10 of for and for and for 10 minutes with a of The was on at for to hours or at for to hours as V. A.J. E. of robust and droplet digital PCR for high mutation detection in circulating DNA.Sci Rep. 2019; PubMed Scopus Google Scholar by at for 10 minutes before on the for in as as four for quality control of a All samples were in and for the and N. Spindler K.L.G. Andersen R.F. Brandslund I. Jakobsen A. Controls to validate plasma samples for cell free DNA quantification.Clin Chim Acta. 2015; 446: 141-146Crossref PubMed Scopus (57) Google T. T. K. A. K. T. of in by droplet digital PCR in patients with 2019; PubMed Scopus Google N. Spindler K.L.G. Andersen R.F. Brandslund I. Jakobsen A. Controls to validate plasma samples for cell free DNA quantification.Clin Chim Acta. 2015; 446: 141-146Crossref PubMed Scopus (57) Google N. C. Spindler K.L.G. The clinical of circulating DNA in cell of the Scopus Google N. C. Spindler K.L.G. The clinical of circulating DNA in cell of the Scopus Google were by Integrated DNA glycine max mRNA for cysteine-rich polycomb-like droplet digital membrane protein blood in a All were by Integrated DNA glycine max mRNA for cysteine-rich polycomb-like droplet digital membrane protein blood with a of were of and were were the of each using and with based on in and control were no in in droplet within the and within the of were with All were in with the for of PCR digital for of digital PCR for Chem. PubMed Scopus Google V. J.A. J. J. M. R. T. J. a of the Chem. PubMed Scopus Google Scholar were using To the of the different cfDNA extraction methods, by was performed to the of the analysis of by for were to the of the cfDNA extraction were The was to the cfDNA quantification using two different This study four different cfDNA extraction methods, including the QIAamp Circulating Nucleic Acid Kit using both the manual and QIAamp MinElute ccfDNA using and QIAsymphony DSP Circulating DNA Kit using The of the extraction methods are in For each extraction method, cfDNA was extracted from plasma on two separate days, using samples obtained from 18 healthy donors. 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This study that the QIAamp Circulating Nucleic Acid Kit using both the manual and outperformed the QIAamp MinElute ccfDNA using the and the QIAsymphony DSP Circulating DNA Kit on the showing higher recovery rates of control DNA and quantity of All four methods robust with no significant in the day-to-day variability of cfDNA four methods extracted cfDNA that the quality control the study The cfDNA no contamination by DNA and was These findings provide a for the utility of cfDNA extracted using methods in clinical applications. This study a that assessed various of plasma cfDNA, including quantity, control and various quality This analysis offers a of the the of most The QIAamp Circulating Nucleic Acid Kit as the with the findings of that have as the choice for cfDNA from R. S. V. A. T. D. A. M. M. F. H. J.P. H. B. S. C. H. P. E. G. K. F. Schuuring E. M. M. T. E. evaluation of circulating cell-free DNA extraction and downstream for the of Chem. PubMed Scopus Google Scholar, R.F. H. Evaluation of commercial for of circulating free Genet. 2018; Full Text Full Text PDF PubMed Scopus Google Scholar, L. K. V. G. F. C. P. of cell-free DNA and quantification of cell-free DNA in Mol 2017; 19: Full Text Full Text PDF PubMed Scopus Google Scholar, S. H. M. Evaluation of commercial for and of circulating cell-free tumor DNA from PubMed Scopus Google Scholar of cfDNA extraction methods have focused on the quantity of cfDNA extracted using various and L. K. V. G. F. C. P. of cell-free DNA and quantification of cell-free DNA in Mol 2017; 19: Full Text Full Text PDF PubMed Scopus Google E. V. A.J. S. and quantification of plasma cell-free DNA using different manual and automated 2022; PubMed Scopus Google Scholar, C. I. M. C. V. L. M. E. M. A. of methods for circulating cell-free DNA using blood from cancer impact on biomarker 2016; PubMed Scopus Google Scholar, S. J. F. A. C. K. P.A. M. H. Evaluation of automated for extraction of circulating cell-free DNA for implementation in Rep. PubMed Scopus Google Scholar, P. P.A. A. van M. J. A. M. Schuuring E. of circulating cell-free DNA extraction methods for downstream analysis in cancer PubMed Scopus Google Scholar the most is to the cfDNA However, is essential to that cfDNA is to factors, including and S. A. M.P. P. of cell-free DNA from affecting liquid 2022; PubMed Scopus Google A.J. A. A.J. van C. C. van T. S. of cell-free DNA from and in and 2019; PubMed Scopus Google Scholar analysis to cfDNA quantity extracted from various donors using different extraction methods should To the of the variability evaluating cfDNA extraction methods, an approach control DNA can be to evaluate the recovery a quantity of control DNA is into the plasma before extraction to the extraction Various control have to cfDNA, and N. Spindler K.L.G. Andersen R.F. Brandslund I. Jakobsen A. Controls to validate plasma samples for cell free DNA quantification.Clin Chim Acta. 2015; 446: 141-146Crossref PubMed Scopus (57) Google A. T. H. V. A. synthetic DNA to evaluate the recovery of cell-free DNA extraction and Chem. PubMed Scopus Google M. A. A. A. P. control to cell free DNA in plasma samples by J 2016; 8: Google Scholar These control DNA are to to cfDNA for clinical applications because are of the of However, using cfDNA from a cell as a control a to cfDNA, such as fragment and with synthetic R. S. V. A. T. D. A. M. M. F. H. J.P. H. B. S. C. H. P. E. G. K. F. Schuuring E. M. M. T. E. evaluation of circulating cell-free DNA extraction and downstream for the of Chem. PubMed Scopus Google Scholar using a be to the choice of the quantification method. methods for cfDNA such as and the DNA both cfDNA and DNA. The by methods can be on the of cfDNA and DNA. To a quantification method, such as can be because can cfDNA and control DNA. for quantification reliable of cfDNA and has as a quantification method R. S. V. A. T. D. A. M. M. F. H. J.P. H. B. S. C. H. P. E. G. K. F. Schuuring E. M. M. T. E. evaluation of circulating cell-free DNA extraction and downstream for the of Chem. PubMed Scopus Google Scholar to yield and recovery efficiency, the quality of cfDNA is for the of downstream clinical with high However, are no for quality control of extracted cfDNA the G. D. S. J. A. A. and quality analyzing cell-free tumor 2019; Sültmann H. A. T. P. V. A. S. for cancer using cell-free DNA: from to and clinical 2018; PubMed Scopus Google Scholar The cfDNA biomarker a minimal of cfDNA, and is to contamination of DNA by proper preanalytical Preanalytical factors such as blood storage and centrifugation are essential for high cfDNA quality and have in van den Broek van J. D. de R. Preanalytical blood sample for cell-free DNA analysis using droplet digital PCR for cancer Med. 2017; PubMed Scopus Google S. F. Mouliere F. Thierry A.R. Circulating cell free DNA: preanalytical Chim Acta. PubMed Scopus Google Scholar the blood samples were within 2 hours for plasma using a double centrifugation regimen, in high DNA quality for cfDNA extraction high cfDNA quality cfDNA extraction methods, the QIAamp MinElute ccfDNA Kit a higher of cfDNA the cfDNA extraction However, because the plasma was to S. Murtaza M. A.J. M.D. cell-free DNA collection and PubMed Scopus Google Scholar, S. K.A. for pre-analytical of plasma Med. 2022; PubMed Google Scholar, L. M. M. D. M. J. K.M. P. A.M. Recommendations for cell-free DNA a consensus of the for and of Mol Full Text Full Text PDF PubMed Scopus Google Scholar assessing the of the cfDNA extraction methods in the of DNA contamination be study by et S. H. M. Evaluation of commercial for and of circulating cell-free tumor DNA from PubMed Scopus Google Scholar that DNA was into plasma the QIAamp Circulating Nucleic Acid Kit higher recovery the QIAamp MinElute ccfDNA This because the QIAamp MinElute ccfDNA Kit a using magnetic whereas the QIAamp Circulating Nucleic Acid Kit DNA both magnetic and methods were for cfDNA However, the choice of was to owing to to the and QIAsymphony This study focused on automated and semiautomated cfDNA extraction research by et R. S. V. A. T. D. A. M. M. F. H. J.P. H. B. S. C. H. P. E. G. K. F. Schuuring E. M. M. T. E. evaluation of circulating cell-free DNA extraction and downstream for the of Chem. PubMed Scopus Google Scholar that QIAsymphony higher recovery of cfDNA with such as the and the for Nucleic Acid that the to the the QIAsymphony was in study to its cfDNA extraction both and healthy donors were in the the cfDNA extraction methods have with plasma samples from cancer recovery efficiency, quantity, and quality were in 18 healthy using methods and The of the cfDNA extraction methods is to be to plasma samples obtained from cancer as has in S. H. M. Evaluation of commercial for and of circulating cell-free tumor DNA from PubMed Scopus Google M. X. X. Q. M. X. L. J. of commercial for and circulating tumor J PubMed Scopus Google Scholar thorough various of plasma cfDNA extraction were including quantity, control and various quality This analysis offers an of the of various methods, the of most comparative the use of the QIAamp Circulating Nucleic Acid Kit, both manual and semiautomated, higher and recovery rates with the fully automated QIAsymphony DSP Circulating DNA Kit on the QIAsymphony and the semiautomated QIAamp MinElute ccfDNA Kit on the The QIAamp Circulating Nucleic Acid Kit offers the of without compromising the quality or quantity of extracted DNA. The for its should be by the specific and clinical in is to be For research or clinical high sample is that using the has because the can samples at a such a sample quantity and a to researchers and clinicians should the specific of their study or clinical the advantages and limitations by each method to ensure the most optimal outcomes.

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