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1 Supplementary Online Content Fumagalli D, Venet D, Ignatiadis M, et al. RNA Sequencing to predict response to neoadjuvant anti-her2 therapy: a secondary analysis of the NeoALTTO randomized clinical trial. Published online September 29, JAMA Oncol. doi: / jamaoncol emethods ereferences etable 1. Patient characteristics in the whole and sequenced cohorts etable 2. Distribution of pcr according to PAM50 subtypes efigure 1. Comparison of ERBB2 gene expression levels determined by RNA Sequencing with classical tests used to define the HER2 status efigure 2. Comparison of ERBB2 gene expression levels in function of the laboratory in which the HER2 standard tests were performed efigure 3. Comparison of ER as determined by IHC and ESR1 gene expression efigure 4. Spearman correlation between single genes and gene expression signatures evaluated in our study efigure 5. Association between clinico-pathologic variables, single genes, and gene expression signatures with pcr by treatment arm efigure 6. Effect of single genes and gene expression signatures on pcr when considering the combination arm versus the joined trastuzumab and lapatinib arms evaluated using an interaction test efigure 7. Effect of single genes and gene expression signatures on pcr when considering the combination versus the trastuzumab arm evaluated using an interaction test efigure 8. Effect of clinico-pathological variables, single genes, gene expression signatures, and treatment on EFS using a univariate model efigure 9. Effect of single genes and gene expression signatures on EFS when considering the combination arm versus the joined trastuzumab and lapatinib arms evaluated using an interaction test This supplementary material has been provided by the authors to give readers additional information about their work.
2 emethods Samples selection A total of 630 baseline frozen samples underwent RNA extraction. For this purpose, snap frozen biopsies obtained at study entrance were first embedded in Optimal Cutting Temperature (OCT) compound and a hematoxylin and eosin (H&E) slide was cut, stained and evaluated for tumor cellularity by a breast cancer pathologist. RNA extraction was performed using the TRIzol method (Life Technologies) following the manufacturer s instructions. The extracted RNA was quantified using the Nanodrop 1000 instrument (Thermo Scientific), and its integrity (RIN: RNA Integrity Number) was assessed using an Agilent 2100 Bioanalyzer (Agilent Technologies). Sample adequacy (as defined by a tumor cellularity 30%), sample integrity (as defined by a RIN 5) and nucleic acid yield (as defined by a RNA quantity 1 µg) were used as quality control criteria. As shown in Figure 1, 219 samples were excluded because of low cellularity, 136 samples because of low RIN, and 12 samples because of low RNA quantity so that 263 samples underwent library preparation. Determination of the HER2 and ER status Only HER2 positive patients could participate in the neoaltto trial. The study required that a HER2 positive result was obtained in a laboratory previously certified for the NeoALTTO study by the NeoALTTO Pathologist Board. A laboratory could be completely, partially or not certified, following the decision of the Pathologist Board. The initial HER2 test was performed locally, by IHC and/or FISH/CISH, regardless of whether the local laboratory was certified. In the case of positive or equivocal results from non-certified local laboratories, slides were sent to the central laboratory (Pathology Department, Vall d Hebron Hospital, Barcelona, Spain) for confirmation prior to randomization. Equivocal results from partially certified laboratories also needed confirmation by the central laboratory prior to randomization in the Neo-ALTTO trial. The American Society of Clinical Oncology and College of American Pathologists (ASCO/CAP) guidelines 1 were used as a basis for defining HER2 positive tumors. HER2 positive tumors were defined as:
3 3+ over expression by IHC (> 30% of invasive tumor cells); 2+ or 3+ (in 30% or less neoplastic cells) over expression by IHC AND in situ hybridization (FISH/CISH) test demonstrating HER2 gene amplification; HER2 gene amplification by FISH/CISH (> 6 HER2 gene copies per nucleus, or a FISH ratio [HER2 gene copies to chromosome 17 signals] over 2.2.) Tumors with equivocal IHC results were defined as 3+ staining of 30% or less of invasive neoplastic cells or 2+ staining. Tumors with equivocal FISH/CISH results were defined as 4 to 6 HER2 gene copies per nucleus or a FISH ratio between 1.8 and 2.2. HER2 negative tumors were defined as tumors with a 0 or 1+ score by IHC and/or lack of HER2 gene amplification (less than 4 copies of HER2 gene per nucleus or a FISH ratio below 1.8). Patients with an overall negative of equivocal result were not eligible for participation in the trial. ER status was assessed only in local laboratories, irrespective of their accreditation, and was considered positive or negative as per local guidelines. RNA sequencing experiments. Starting from 1 µg of total RNA, rrna was depleted using the Ribo-Zero Magnetic Kit (Epicentre) according to the manufacturer s instruction. Following purification, the mrna was fragmented. The cleaved RNA fragments were copied into first strand cdna using reverse transcriptase and random primers. This was followed by second strand cdna synthesis and purification using the AMPure XP beads (Agencourt BioSciences Corporation). The cdna fragments underwent an end repair process, the addition of a single A nucleotide and ligation of the adapters. The products were purified using the AMPure XP beads and enriched after digestion of the second strand with PCR to create the final cdna library. Another purification step using the AMPure XP beads followed. Libraries quality control and quantification were performed using the Fragment Analyzer (Advanced Analytical) and the Qubit (Life Technologies). Nine samples failed the library construction step. The remaining 254 (Figure 1) libraries were pooled with three libraries per pool. Clusters were generated in a cbot Cluster Generation System using the Kits TruSeq PE Cluster Kit v3-cbot-
4 HS and HiSeq PE Cluster Kit v4 cbot and sequenced on the Illumina HiSeq 2500 platform with a 2x100 base pairs paired-end mode.
5 ereferences Wolff AC, Hammond MEH, Schwartz JN, et al. American Society of Clinical Oncology/College of American Pathologists Guideline Recommendations for Human Epidermal Growth Factor Receptor 2 Testing in Breast Cancer. J Clin Oncol 2007; 25:
6 etable 1. Patient characteristics in the whole and sequenced cohorts Characteristics Whole cohort (N=455) Sequenced cohort (N=254) p-value Age Median Range Tumor Size >=T3 181 (40%) 103 (41%) 0.77 T2 274 (60%) 151 (59%) Nodal Status >=N2, Nx or missing 72 (16%) 38 (15%) 0.61 N0/1 383 (84%) 216 (85%) Hormone Receptor Status Treatment arm negative 223 (49%) 117 (46%) 0.19 positive 232 (51%) 137 (54%) L 154 (34%) 89 (35%) 0.68 T 149 (33%) 79 (31%) L+T 152 (33%) 86 (34%) pcr No 295 (65%) 166 (65%) 0.84 Yes 160 (35%) 88 (35%) Comparison of the clinico-pathologic and treatment characteristics of the whole cohort of patients randomized in the neoaltto trial and the sub-study cohort analyzed in this project. L: Lapatinib; T: trastuzumab
7 etable 2. Distribution of pcr according to PAM50 subtypes Basal Her2 Luminal A Luminal B Normal N % 9% 43% 23% 16% 8% %pcr 38% 52% 17% 17% 24% Classification of the sub-study population according to the subtypes defined by the PAM50 classifier and distribution of observed pcr according to the subtype.
8 efigure 1. Comparison of ERBB2 gene expression levels determined by RNA Sequencing with classical tests used to define the HER2 status A) Comparison between ERBB2 gene expression levels with IHC, using the % stained cells and B) with FISH ratios.
9 efigure 2. Comparison of ERBB2 gene expression levels in function of the laboratory in which the HER2 standard tests were performed ERBB2 expression (FPKM) ERBB2 expression (FPKM) Local lab Central lab Central testing Local testing ESR1 expression (FPKM) A A) ERBB2 expression levels according to where the HER2 standard tests were performed (central testing vs. local testing). B) ERBB2 versus ESR1 expression levels with samples colored according to laboratories in which the HER2 standard tests were performed (red:central; black:local). Red line denotes the cutoff used to determine low versus high expression levels of ERBB2. B
10 efigure 3. Comparison of ER as determined by IHC and ESR1 gene expression A) ESR1 expression levels in the ER+ and ER- patients determined by local IHC. B) ERBB2 and ESR1 gene expression levels determined by RNA sequencing in the ER+ (black) and ER- (red) patients determined by local IHC.
11 efigure 4. Spearman correlation between single genes and gene expression signatures evaluated in our study The color indicates the direction of the correlation (red: anti-correlation; blue: direct correlation); the shape of the ovals indicates the strength of the correlation. Only significant correlations are shown (p<0.05).
12 efigure 5. Association between clinico-pathologic variables, single genes, and gene expression signatures with pcr by treatment arm A) Lapatinib; B) Trastuzumab; C) Combination. Blue represents significant p values.
13 efigure 6. Effect of single genes and gene expression signatures on pcr when considering the combination arm versus the joined trastuzumab and lapatinib arms evaluated using an interaction test Blue indicates effect across arms, red indicates effect specific to the combination arm; dark colors indicate significant correlation.
14 efigure 7. Effect of single genes and gene expression signatures on pcr when considering the combination versus the trastuzumab arm evaluated using an interaction test Blue indicates effect across arms, red indicates effect specific to the combination arm; dark colors indicate significant correlation.
15 efigure 8. Effect of clinico-pathological variables, single genes, gene expression signatures, and treatment on EFS using a univariate model Blue represents significant p values.
16 efigure 9. Effect of single genes and gene expression signatures on EFS when considering the combination arm versus the joined trastuzumab and lapatinib arms evaluated using an interaction test Blue indicates effect across arms, red indicates effect specific to the combination arm; dark colors indicate significant correlation.
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