Non-invasive prenatal detection of chromosome aneuploidies using next generation sequencing: First steps towards clinical application



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Non-invasive prenatal detection of chromosome aneuploidies using next generation sequencing: First steps towards clinical application PD Dr. rer. nat. Markus Stumm Zentrum für Pränataldiagnostik Kudamm-199 stumm@kudamm-199.de

Prenatal Diagnosis and NGS - Why? Dennis Lo In 1997 Lo et al. reported that circulating cell-free fetal (ccff) DNA is present in the plasma of pregnant woman. ccff DNA can be detected as early as the 32nd day of gestation. ccff DNA ranges between 2% and 40% with a mean around 10% across varying gestational ages.

Massively parallel genomic sequencing From 2008 to 2010 three cohort studies have shown that MPGS of ccff-dna can identify plasma samples from woman carrying an aneuploid fetus compared to samples from women with euploid fetuses.

6/6 Euploid ; 9/9 Trisomy 21; 1/1 Trisomy 13; 2/2 Trisomy 18 14/14 Euploid 14/14 Trisomy 21

The Quantification Problem Only a small amount of serum DNA is of fetal offspring! If a maternal plasma probe contains e.g. 100 copies of chromosome 21 specific sequences, in an euploid pregnancy a maximum of 10 copies are fetal (90 maternal and 10 fetal) Accordingly, a trisomy 21 pregnancy contains 105 copies of chromosome 21 specific sequences (90 maternal and 15 fetal) In the maternal plasma of a trisomy 21 pregnancy, the amount of chromosome 21 specific DNA is increased only by the factor 1.05 Can massively parallel genomic sequencing detect that minimal quantitative difference reliably?

Proof of Principle Study Next Generation Sequencing (NGS) in Non Invasive Prenatal Diagnosis (NIPD) The diagnostic performance of NGS was compared to full conventional karyotyping Positive Vote from the Ethical Committee of the Ärztekammer Berlin in October 2009 Cooperation: Zentrum für Pränataldiagnostik und Humangenetik Kudamm 199 in Berlin and LifeCodexx AG in Konstanz

Study Group Patient recruitment: Zentrum für Pränataldiagnostik und Humangenetik Kudamm-199 Berlin Patients inclusion criteria: Singleton pregnancies in first and second trimester with clinical indications for chorionic villi sampling or amniocentesis. Patient informed consent was obtained for peripheral blood sampling and for the inclusion of karyotype results.

Sample processing Peripheral venous blood samples were collected (5-10 ml EDTA blood) and plasma samples were harvested and frozen at -20 C Plasma samples were sent to LifeCodexx by overnight courier while kept frozen Cell free DNA isolation using QIAmp Circulating Nucleic Acid Kit

Library Preparation Library construction with Ilumina V2-adapters following the protocol for ChIP samples Libraries were amplified using a 12 cycle PCR step The adapter ligated fragments were size selected in the range of 150-300 bp Quality control and quantification using a High Sensitivity DNA Kit on the Agilent 2100 Bioanalyzer Molar quantification was done with the Qubit Fluorometer Libraries compatible with Paired-End (PE) sequencing were loaded for monoplex analysis on Illumina Paired End Flow Cells

Cell free DNA sequencing Cluster Generation with Bridge Amplification Pyrosequencing on the Illumina Genome Analyzer IIx in single read mode Read length 36 bp

35.000.000 32.500.000 30.000.000 27.500.000 25.000.000 22.500.000 20.000.000 17.500.000 15.000.000 12.500.000 10.000.000 7.500.000 5.000.000 2.500.000 0 S03 S04 S07 S12 S14 S19 S20 NGS-Results 1 42 samples were sequenced on the Genome Analyzer IIx S21 S23 S26 S28 S29 S30 S31 sequenced reads S32 S33 S34 S35 S36 S37 S38 S39 S40 S41 S42 S43 S44 S45 S46 S47 S48 S49 S50 S51 S55 Euploid T21 S56 S57 S60 S61 S62 S63 S64 average of 14.461.145 reads average genome coverage: ~25%; depth 1

Sequencing data analysis Processing of the sequencing data with the use of a bio-informatics algorithm adapted from Chiu et al. (PNAS 2008) The first 32 bp of each read were aligned to the repeat-masked human genomic reference sequence NCBI build 36 (hg18)

NGS-Results 2 average of 5.857.141 unique mapped reads without any mismatch (UMR-0mm) UMR-0mm mapped to human chromosomes 600.000 500.000 400.000 300.000 200.000 100.000 0 #X: 243.525 #21: 74.077 #Y: 4.132 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 X Y Number of counted reads correlates to the size of the chromosomes

Sequencing data analysis Disease status determination by z- score calculation: 1. the fractional genomic representation of a specific chromosome (% chrn) was determined by dividing the number of unique counts for that specific chromosome by the number of unique counts of all chromosomes 2. % chrn was standardized by subtracting the mean % chrn of a control group and dividing by the SD of the same control group A z-score higher than >3 was used as cut-off value for aneuploid pregnancies

21 18 15 12 9 6 3 0-3 -6 NGS-Results 3 z-score chromosome 21 Euploid 2,79 1,88-1,76-2,67 All eight trisomy 21 cases were correctly identified with a z-score >3 0,97 0,06-0,85 T21 18,25 9,15 4,61 3,70 6,43

50% 40% 30% 20% 10% 0% -10% -20% -30% -40% 6% 4% 2% 0% -2% -4% -6% -8% % UMR-0mm chromosome Y S44 female male %Y gg XX (hg18 rm) %Y gg XY (hg18 rm) % UMR-0mm chromosome X NGS-Results 4 S44 female male %X gg XX (hg18 rm) %X gg XY (hg18 rm) Comparing the fractional genomic representation of the gonosomes (% chrx and % chry) allows also the detection of the missing X chromosome in a monosomy X pregnancy. % chry comparable to a female pregnancy combined with a % chrx comparable to a male pregnancy = Monosomy X

Summary 42 cell free serum DNA samples were analysed from singleton pregnancies in first and second trimester with clinical indications for chorionic villi sampling or amniocentesis. Eight cases with trisomy 21 cases and one case with monosomy X were detected by next generation sequencing and confirmed by conventional karyotyping.

Further Improvements The detection of other aneuploidies, e.g. trisomy 13 and trisomy 18, is problematical: Change to the HiSeq 2000 system and enrichment strategies will increase the number of reads, additional improvements in bioinformatics will further increase the diagnostic sensitivity. The determination of the amount of fetal DNA in the maternal plasma sample is necessary for quality control: Combined methylation status- and SNP-analyses are in progress NGS is currently expensive (~1000 / sample): Probe multiplexing (5x) on the HiSeq 2000 system and further automatic control will reduce the costs.

Studies Patients Sensitivity Specifity Inclusion criteria Sample collection DNA extraction Sequencing Bio-IT analysis References QC Chiu et al. 2011 232 100% 97,9% increases risk patients phlebotomy prior invasiv procedure full karyotyping 5-10 ml EDTA-blood 2-4 ml plasma Qiamp DSP DNA blood mini Kit GAIIX; 2-plexing z-score: =/>3 - T21 hg18, repeat-masked U-0-1-0-0 with 0MM 82 male euploid 2,3 Mill. Reads DNA: QRT-PCR: ß-globin Ehrich et al. 2011 449 100% 99,7% increases risk patients phlebotomy prior invasiv procedure full Karyotyping; FISH, QF- PCR 10 ml EDTA-blood >3,5 ml plasma QIAmp circulating nucleic acid Kit GAIIx; 4-plexing z-score: =/>2,5 - T21 hg 19, nonrepeat-masked 1 MM 24 euploid 3-5 Mill. reads DNA: fetal fractio: 3,9% LifeCodexx 500 aim: 100% aim: 99% increased risk patients phlebotomy prior invasive procedure full karyotyping 10 ml EDTA-blood >3,5 ml plasma QIAmp circulating nucleic acid Kit HiSeq 2000, 5-plexing z-score: =/>3 - T21 hg18, repeat-masked UMR-0mm 15+ euploid 10 Mill. reads 90% UMR-0mm Multi-center study in Progress

7-2010 PD Dr. Michael Entezami Dr. Wera Hofmann Nastasja Trunk Martina Beck Julia Löcherbach w.hofmann@lifecodexx.com Prof. Dr. Rolf Becker PD Dr. Markus Stumm Prof. Rolf-Dieter Wegner stumm@kudamm-199.de Supported by the German Federal Ministry of Education and Research (BMBF); EP 091488