Droplet Digital PCR

Nunes V. Cazzaniga G. Biondi A.

An update on PCR use for minimal residual disease monitoring in acute lymphoblastic leukemia.

Expert Rev Mol Diagn. 17: 953-963van Dongen J.J. van der Velden V.H.J. Brüggemann M. Orfao A.

Minimal residual disease diagnostics in acute lymphoblastic leukemia: need for sensitive, fast, and standardized technologies.

Blood. 125: 3996-4009Brüggemann M. Raff T. Kneba M.

Has MRD monitoring superseded other prognostic factors in adult ALL?.

Blood. 120: 4470-4481Borowitz M.J. Devidas M. Hunger S.P. Bowman W.P. Carroll A.J. Carroll W.L. Linda S. Martin P.L. Pullen D.J. Viswanatha D. Willman C.L. Winick N. Camitta B.M. Children’s Oncology Group

Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia and its relationship to other prognostic factors: a Children's Oncology Group study.

Blood. 111: 5477-5485Eckert C. Hagedorn N. Sramkova L. Mann G. Panzer-Grümayer R. Peters C. Bourquin J.-P. Klingebiel T. Borkhardt A. Cario G. Alten J. Escherich G. Astrahantseff K. Seeger K. Henze G. von Stackelberg A.

Monitoring minimal residual disease in children with high-risk relapses of acute lymphoblastic leukemia: prognostic relevance of early and late assessment.

Leukemia. 29: 1648-1655Eckert C. Henze G. Seeger K. Hagedorn N. Mann G. Panzer-Grumayer R. Peters C. Klingebiel T. Borkhardt A. Schrappe M. Schrauder A. Escherich G. Sramkova L. Niggli F. Hitzler J. von Stackelberg A.

Use of allogeneic hematopoietic stem-cell transplantation based on minimal residual disease response improves outcomes for children with relapsed acute lymphoblastic leukemia in the intermediate-risk group.

J Clin Oncol. 31: 2736-2742Flohr T. Schrauder A. Cazzaniga G. Panzer-Grümayer R. van der Velden V. Fischer S. Stanulla M. Basso G. Niggli F.K. Schäfer B.W. Sutton R. Koehler R. Zimmermann M. Valsecchi M.G. Gadner H. Masera G. Schrappe M. van Dongen J.J. Biondi A. Bartram C.R. International BFM Study Group (I-BFM-SG)

Minimal residual disease-directed risk stratification using real-time quantitative PCR analysis of immunoglobulin and T-cell receptor gene rearrangements in the international multicenter trial AIEOP-BFM ALL 2000 for childhood acute lymphoblastic leukemia.

Leukemia. 22: 771-782Cavé H. van der Werff ten Bosch J. Suciu S. Guidal C. Waterkeyn C. Otten J. Bakkus M. Thielemans K. Grandchamp B. Vilmer E.

Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia. European Organization for Research and Treatment of Cancer–Childhood Leukemia Cooperative Group.

N Engl J Med. 339: 591-598Bader P. Kreyenberg H. von Stackelberg A. Eckert C. Salzmann-Manrique E. Meisel R. Poetschger U. Stachel D. Schrappe M. Alten J. Schrauder A. Schulz A. Lang P. Müller I. Albert M.H. Willasch A.M. Klingebiel T.E. Peters C.

Monitoring of minimal residual disease after allogeneic stem-cell transplantation in relapsed childhood acute lymphoblastic leukemia allows for the identification of impending relapse: results of the ALL-BFM-SCT 2003 trial.

J Clin Oncol. 33: 1275-1284Eckert C. von Stackelberg A. Seeger K. Groeneveld T.W.L. Peters C. Klingebiel T. Borkhardt A. Schrappe M. Escherich G. Henze G.

Minimal residual disease after induction is the strongest predictor of prognosis in intermediate risk relapsed acute lymphoblastic leukaemia—long-term results of trial ALL-REZ BFM P95/96.

Eur J Cancer. 49: 1346-1355Bader P. Kreyenberg H. Henze G.H.R. Eckert C. Reising M. Willasch A. Barth A. Borkhardt A. Peters C. Handgretinger R. Sykora K.-W. Holter W. Kabisch H. Klingebiel T. von Stackelberg A. ALL-REZ BFM Study Group

Prognostic value of minimal residual disease quantification before allogeneic stem-cell transplantation in relapsed childhood acute lymphoblastic leukemia: the ALL-REZ BFM Study Group.

J Clin Oncol. 27: 377-384Steinbach D. Bader P. Willasch A. Bartholomae S. Debatin K.-M. Zimmermann M. Creutzig U. Reinhardt D. Gruhn B.

Prospective validation of a new method of monitoring minimal residual disease in childhood acute myelogenous leukemia.

Clin Cancer Res. 21: 1353-1359van der Velden V.H.J. Brüggemann M. Hoogeveen P.G. de Bie M. Hart P.G. Raff T. Pfeifer H. Lüschen S. Szczepański T. van Wering E.R. Kneba M. van Dongen J.J.M.

TCRB gene rearrangements in childhood and adult precursor-B-ALL: frequency, applicability as MRD-PCR target, and stability between diagnosis and relapse.

Leukemia. 18: 1971-1980Brüggemann M. van der Velden V.H.J. Raff T. Droese J. Ritgen M. Pott C. Wijkhuijs A.J. Gökbuget N. Hoelzer D. van Wering E.R. van Dongen J.J. Kneba M.

Rearranged T-cell receptor beta genes represent powerful targets for quantification of minimal residual disease in childhood and adult T-cell acute lymphoblastic leukemia.

Leukemia. 18: 709-719van der Velden V.H.J. de Bie M. van Wering E.R. van Dongen J.J.M.

Immunoglobulin light chain gene rearrangements in precursor-B-acute lymphoblastic leukemia: characteristics and applicability for the detection of minimal residual disease.

Haematologica. 91: 679-682van der Velden V.H.J. van Dongen J.J.M.

MRD detection in acute lymphoblastic leukemia patients using Ig/TCR gene rearrangements as targets for real-time quantitative PCR.

Methods Mol Biol. 538: 115-150

Real-time PCR to detect minimal residual disease in childhood ALL.

Methods Mol Med. 91: 175-182van der Velden V.H.J. Hochhaus A. Cazzaniga G. Szczepanski T. Gabert J. van Dongen J.J.M.

Detection of minimal residual disease in hematologic malignancies by real-time quantitative PCR: principles, approaches, and laboratory aspects.

Leukemia. 17: 1013-1034Malec M. van der Velden V.H.J. Björklund E. Wijkhuijs J.M. Söderhall S. Mazur J. Björkholm M. Porwit-MacDonald A.

Analysis of minimal residual disease in childhood acute lymphoblastic leukemia: comparison between RQ-PCR analysis of Ig/TcR gene rearrangements and multicolor flow cytometric immunophenotyping.

Leukemia. 18: 1630-1636van der Velden V.H.J. Panzer-Grümayer E.R. Cazzaniga G. Flohr T. Sutton R. Schrauder A. Basso G. Schrappe M. Wijkhuijs J.M. Konrad M. Bartram C.R. Masera G. Biondi A. van Dongen J.J.M.

Optimization of PCR-based minimal residual disease diagnostics for childhood acute lymphoblastic leukemia in a multi-center setting.

Leukemia. 21: 706-713van der Velden V.H.J. Cazzaniga G. Schrauder A. Hancock J. Bader P. Panzer-Grumayer E.R. Flohr T. Sutton R. Cave H. Madsen H.O. Cayuela J.M. Trka J. Eckert C. Foroni L. Zur Stadt U. Beldjord K. Raff T. van der Schoot C.E. van Dongen J.J.M. European Study Group on MRD detection in ALL (ESG-MRD-ALL)

Analysis of minimal residual disease by Ig/TCR gene rearrangements: guidelines for interpretation of real-time quantitative PCR data.

Leukemia. 21: 604-611Della Starza I. Chiaretti S. De Propris M.S. Elia L. Cavalli M. De Novi L.A. Soscia R. Messina M. Vitale A. Guarini A. Foa R.

Minimal residual disease in acute lymphoblastic leukemia: technical and clinical advances.

Front Oncol. 9: 726Yuan D. Cui M. Yu S. Wang H. Jing R.

Droplet digital PCR for quantification of PML-RAR[alpha] in acute promyelocytic leukemia: a comprehensive comparison with real-time PCR.

Anal Bioanal Chem. 411: 895-903Della Starza I. Nunes V. Cavalli M. De Novi L.A. Ilari C. Apicella V. Vitale A. Testi A.M. Del Giudice I. Chiaretti S. Foà R. Guarini A.

Comparative analysis between RQ-PCR and digital-droplet-PCR of immunoglobulin/T-cell receptor gene rearrangements to monitor minimal residual disease in acute lymphoblastic leukaemia.

Br J Haematol. 174: 541-549Hindson C.M. Chevillet J.R. Briggs H.A. Gallichotte E.N. Ruf I.K. Hindson B.J. Vessella R.L. Tewari M.

Absolute quantification by droplet digital PCR versus analog real-time PCR.

Nat Methods. 10: 1003-1005Jennings L.J. George D. Czech J. Yu M. Joseph L.

Detection and quantification of BCR-ABL1 fusion transcripts by droplet digital PCR.

J Mol Diagn. 16: 174-179Drandi D. Kubiczkova-Besse L. Ferrero S. Dani N. Passera R. Mantoan B. Gambella M. Monitillo L. Saraci E. Ghione P. Genuardi E. Barbero D. Omedè P. Barberio D. Hajek R. Vitolo U. Palumbo A. Cortelazzo S. Boccadoro M. Inghirami G. Ladetto M.

Minimal residual disease detection by droplet digital PCR in multiple myeloma, mantle cell lymphoma, and follicular lymphoma: a comparison with real-time PCR.

J Mol Diagn. 17: 652-660Campomenosi P. Gini E. Noonan D.M. Poli A. D'Antona P. Rotolo N. Dominioni L. Imperatori A.

A comparison between quantitative PCR and droplet digital PCR technologies for circulating microRNA quantification in human lung cancer.

BMC Biotechnol. 16: 60Brunetti C. Anelli L. Zagaria A. Minervini A. Minervini C.F. Casieri P. Coccaro N. Cumbo C. Tota G. Impera L. Orsini P. Specchia G. Albano F.

Droplet digital PCR is a reliable tool for monitoring minimal residual disease in acute promyelocytic leukemia.

J Mol Diagn. 19: 437-444Park H. Shin D.-Y. Kim I. Sohn S.-K. Koh Y. Lee J.-H. Lee K.-H. Kim D.-Y. Kim H.-J. Ahn J.-S. Lee J.-O. Bang S.-M. Cheong J.-W. Park S.-G. Park S. Lee Y.J. Ahn S.-Y.

Use of droplet digital polymerase chain reaction for detecting minimal residual disease: a prospective multi-institutional study.

In Vivo. 33: 2273-2280Della Starza I. Cavalli M. De Novi L.A. Genuardi E. Mantoan B. Drandi D. Barbero D. Ciabatti E. Grassi S. Gazzola A. Mannu C. Agostinelli C. Piccaluga P.P. Bomben R. Degan M. Gattei V. Guarini A. Foà R. Galimberti S. Ladetto M. Ferrero S. Del Giudice I. Fondazione Italiana Linfomi (FIL) MRD Network

Minimal residual disease (MRD) in non-Hodgkin lymphomas: interlaboratory reproducibility on marrow samples with very low levels of disease within the FIL (Fondazione Italiana Linfomi) MRD Network.

Hematol Oncol. 37: 368-374Drandi D. Ferrero S. Ladetto M.

Droplet digital PCR for minimal residual disease detection in mature lymphoproliferative disorders.

Methods Mol Biol. 1768: 229-256Dworzak M.N. Panzer-Grümayer E.R.

Flow cytometric detection of minimal residual disease in acute lymphoblastic leukemia.

Leuk Lymphoma. 44: 1445-1455Gaipa G. Buracchi C. Biondi A.

Flow cytometry for minimal residual disease testing in acute leukemia: opportunities and challenges.

Expert Rev Mol Diagn. 18: 775-787Karawajew L. Dworzak M. Ratei R. Rhein P. Gaipa G. Buldini B. Basso G. Hrusak O. Ludwig W.-D. Henze G. Seeger K. von Stackelberg A. Mejstrikova E. Eckert C.

Minimal residual disease analysis by eight-color flow cytometry in relapsed childhood acute lymphoblastic leukemia.

Haematologica. 100: 935-944Drandi D. Alcantara M. Benmaad I. Söhlbrandt A. Lhermitte L. Zaccaria G. Ferrante M. Genuardi E. Mantoan B. Villarese P. Cheminant M. Starza I.D. Ciabatti E. Bomben R. Jimenez C. Callanan M. Abdo C. Eckert C. Ribrag V. Cortelazzo S. Dreyling M. Hermine O. Delfau-Larue M.-H. Pott C. Ladetto M. Ferrero S. Macintyre E.

Droplet digital PCR quantification of mantle cell lymphoma follow-up samples from four prospective trials of the European MCL Network.

Hemasphere. 4: e347Huggett J.F. Foy C.A. Benes V. Emslie K. Garson J.A. Haynes R. Hellemans J. Kubista M. Mueller R.D. Nolan T. Pfaffl M.W. Shipley G.L. Vandesompele J. Wittwer C.T. Bustin S.A.

The digital MIQE guidelines: minimum information for publication of quantitative digital PCR experiments.

Clin Chem. 59: 892-902Huggett J.F. Cowen S. Foy C.A.

Considerations for digital PCR as an accurate molecular diagnostic tool.

Clin Chem. 61: 79-88Corbisier P. Pinheiro L. Mazoua S. Kortekaas A.-M. Chung P.Y.J. Gerganova T. Roebben G. Emons H. Emslie K.

DNA copy number concentration measured by digital and droplet digital quantitative PCR using certified reference materials.

Anal Bioanal Chem. 407: 1831-1840

Measurement in medicine—the analysis of method comparison studies.

J R Stat Soc. 32: 307-317

Understanding Bland Altman analysis.

Biochem Med (Zagreb). 25: 141-151

Digital assays part I: partitioning statistics and digital PCR.

SLAS Technol. 22: 369-386Della Starza I. Nunes V. Lovisa F. Silvestri D. Cavalli M. Garofalo A. Campeggio M. De Novi L.A. Soscia R. Oggioni C. Mussolin L. Biondi A. Guarini A. Valsecchi M.G. Conter V. Biffi A. Basso G. Foà R. Cazzaniga G.

Droplet digital PCR improves IG-/TR-based MRD risk definition in childhood B-cell precursor acute lymphoblastic leukemia.

Hemasphere. 5: e543Del Giudice I. Raponi S. Della Starza I. De Propris M.S. Cavalli M. De Novi L.A. Cappelli L.V. Ilari C. Cafforio L. Guarini A. Foà R.

Minimal residual disease in chronic lymphocytic leukemia: a new goal?.

Front Oncol. 9: 689Bill M. Grimm J. Jentzsch M. Kloss L. Goldmann K. Schulz J. Beinicke S. Häntschel J. Cross M. Vucinic V. Pönisch W. Behre G. Franke G.-N. Lange T. Niederwieser D. Schwind S.

Digital droplet PCR-based absolute quantification of pre-transplant NPM1 mutation burden predicts relapse in acute myeloid leukemia patients.

Ann Hematol. 97: 1757-1765Campana D. Neale G.A. Coustan-Smith E. Pui C.H.

Detection of minimal residual disease in acute lymphoblastic leukemia: the St Jude experience.

Leukemia. 15: 278-279Coustan-Smith E. Gajjar A. Hijiya N. Razzouk B.I. Ribeiro R.C. Rivera G.K. Rubnitz J.E. Sandlund J.T. Andreansky M. Hancock M.L. Pui C.-H. Campana D.

Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia after first relapse.

Leukemia. 18: 499-504Denys B. van der Sluijs-Gelling A.J. Homburg C. van der Schoot C.E. de Haas V. Philippé J. Pieters R. van Dongen J.J.M. van der Velden V.H.J.

Improved flow cytometric detection of minimal residual disease in childhood acute lymphoblastic leukemia.

Leukemia. 27: 635-641Gaipa G. Cazzaniga G. Valsecchi M.G. Panzer-Grümayer R. Buldini B. Silvestri D. Karawajew L. Maglia O. Ratei R. Benetello A. Sala S. Schumich A. Schrauder A. Villa T. Veltroni M. Ludwig W.-D. Conter V. Schrappe M. Biondi A. Dworzak M.N. Basso G.

Time point-dependent concordance of flow cytometry and real-time quantitative polymerase chain reaction for minimal residual disease detection in childhood acute lymphoblastic leukemia.

Haematologica. 97: 1582-1593Garand R. Beldjord K. Cavé H. Fossat C. Arnoux I. Asnafi V. Bertrand Y. Boulland M.-L. Brouzes C. Clappier E. Delabesse E. Fest T. Garnache-Ottou F. Huguet F. Jacob M.-C. Kuhlein E. Marty-Grès S. Plesa A. Robillard N. Roussel M. Tkaczuk J. Dombret H. Macintyre E. Ifrah N. Béné M.C. Baruchel A.

Flow cytometry and IG/TCR quantitative PCR for minimal residual disease quantitation in acute lymphoblastic leukemia: a French multicenter prospective study on behalf of the FRALLE, EORTC and GRAALL.

Leukemia. 27: 370-376Irving J. Jesson J. Virgo P. Case M. Minto L. Eyre L. Noel N. Johansson U. Macey M. Knotts L. Helliwell M. Davies P. Whitby L. Barnett D. Hancock J. Goulden N. Lawson S. UKALL Flow MRD Group, UK MRD Steering Group

Establishment and validation of a standard protocol for the detection of minimal residual disease in B lineage childhood acute lymphoblastic leukemia by flow cytometry in a multi-center setting.

Haematologica. 94: 870-874Neale G.A.M. Coustan-Smith E. Stow P. Pan Q. Chen X. Pui C.-H. Campana D.

Comparative analysis of flow cytometry and polymerase chain reaction for the detection of minimal residual disease in childhood acute lymphoblastic leukemia.

Leukemia. 18: 934-938Pulsipher M.A. Han X. Maude S.L. Laetsch T.W. Qayed M. Rives S. Boyer M.W. Hiramatsu H. Yanik G.A. Driscoll T. Myers G.D. Bader P. Baruchel A. Buechner J. Stefanski H.E. Kalfoglou C. Nguyen K. Waldron E.R. Thudium Mueller K. Maier H.J. Kari G. Grupp S.A.

Next-generation sequencing of minimal residual disease for predicting relapse after tisagenlecleucel in children and young adults with acute lymphoblastic leukemia.

Blood Cancer Discov. 3: 66-81

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