PMC:7574920 / 42878-58709 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7574920","sourcedb":"PMC","sourceid":"7574920","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7574920","text":"MATERIALS AND METHODS\n\nStudy design\nThe intent of this study was to develop a clinical method for detecting SARS-CoV-2 RNA in RNA samples isolated from pharyngeal swab specimens from individuals being tested for COVID-19. We used pseudo-anonymized surplus RNA sample material that had been collected for clinical diagnosis of SARS-CoV-2 infection by RT-qPCR carried out by the diagnostic laboratory of Heidelberg University Hospital. Such reuse of material is in accordance with German regulations, which allow development and improvement of diagnostic assays using patient samples collected specifically to perform the testing in question. Pharyngeal swab specimens provided to us were either collected through the nose (nasopharyngeal) or the mouth (oropharyngeal), or sometimes one swab was used to collect both.\nOur study was designed to investigate the sensitivity and specificity of a colorimetric RT-LAMP assay and to evaluate its suitability as an alternative to RT-qPCR testing for detecting SARS-CoV-2 viral RNA in RNA isolated from pharyngeal swab specimens. This study was conducted in Heidelberg, Germany in March and April of 2020. The study was designed to first evaluate different existing primer sets for RT-LAMP reactions and to use them for (i) detection of SARS-CoV-2 RNA in RNA isolated from pharyngeal swabs and (ii) detection of SARS-CoV-2 RNA directly from swab specimens without prior RNA isolation. All RNA samples used were pseudo-anonymized surplus material from the Heidelberg University Hospital diagnostic laboratory, and RT-qPCR results for these RNA samples were retrieved from the laboratory’s database only after the samples had been analyzed by the RT-LAMP assay. The study design was to conduct RT-LAMP testing until sufficient samples (at least several hundreds) had been analyzed to obtain a conclusive result. We also designed a deep sequencing-based method to validate the outcome of the RT-LAMP reactions using a Tn5 transposase–based fully scalable barcoding strategy (LAMP-sequencing).\n\nClinical sample handling\nSpecimens were collected as nasopharyngeal and oropharyngeal flocked swabs in Amies medium (eSwab, Copan Italia). The sample collection happened as part of the routine operation of Heidelberg University Hospital and at public testing stations set up by the City of Heidelberg (fig. S1). Collected samples were transported in sterile containers, delivered to the diagnostic laboratory within a few hours, and then examined directly or stored at 4°C until further processing. Samples were processed in a biosafety level 2 cabinet until inactivation by heat or mixing with a lysis buffer.\n\nRNA isolation and RT-qPCR\nThe standard diagnostic pipeline of the hospital laboratory was as follows: RNA was isolated from nasopharyngeal and oropharyngeal swab specimens using QIAGEN kits (QIAGEN, Hilden, Germany); either automated on the QIASymphony (DSP Virus/Pathogen Mini Kits) or QIAcube (QIAamp Viral RNA Mini Kits) devices or manually (QIAamp Viral RNA Mini Kits). Please note that the QiaCube uses a sample volume of 140 μl and an elution volume of 100 μl, whereas the QiaSymphony uses a sample volume of 200 μl and an elution volume of 115 μl. RT-qPCR for the quantification of the SARS-CoV-2 viral genome was performed using kits and reagents from TIB MOLBIO Syntheselabor, Berlin, Germany. The kits were used according to the manufacturer’s instruction and contained the primer/probe sets developed based on the published Sarbeco primer set (15). Per 20-μl reaction, the master mix contained 5.4 μl of RNAse free water, 4.0 μl of LightCycler Multiplex RNA Virus Master (Roche, Basel, Switzerland), 0.5 μl of LightMix Modular SARS and Wuhan CoV E gene (cat. no. 53-0776-96; TIB MOLBIOL Syntheselabor GmbH, Berlin, Germany) or LightMix Modular SARS and Wuhan CoV N gene (cat. no. 53-0775-96; TIB MOLBIOL), 0.5 μl of LightMix Modular EAV RNA Extraction Control (cat. no. 66-0909-96; TIB MOLBIOL), and 0.1 μl of reverse transcriptase enzyme (LightCycler Multiplex RNA Virus Master, Roche, Basel, Switzerland). The master mix (10 μl) was distributed per reaction into 96-well plates, and 10 μl of purified RNA was added per well. The performance of the RT-qPCR was validated using a positive control for the E gene. A total of 103 molecules of E gene RNA per RT-qPCR reaction correspond to a CT ≈ 30.\n\nRT-LAMP primer design and positive control\nThe RT-LAMP primer sets used in this study have been designed by Zhang et al. (11) against ORF1a and N gene and were synthesized by Sigma-Aldrich (synthesis scale, 0.025 μmol; purification, desalt; solution, water). The sequences and the concentrations of each oligonucleotide in the 10× primer mix used for the RT-LAMP assay can be found in table S1.\nAn RNA-positive control for the N gene was amplified from a short fragment from 2019-nCoV_N_Positive control plasmid [Integrated DNA Technologies (IDT), 10006625] with oligonucleotides T7-GeneN-Fragment.for and GeneN-Fragment.rev including the T7 promoter and a subsequent IVT with the MEGAscript T7 Kit (Invitrogen) purified using the RNeasy MinElute Cleanup Kit (QIAGEN).\n\nLiquid handling using 96-well plates and precautions taken to prevent contamination\nTo prevent cross-contamination, we have taken several precautions. The 10× primer mix was prepared with nuclease-free water (AM9937, Ambion) and stored in aliquots at −20°C. To set up an RT-LAMP test, the RT-LAMP master mix was prepared freshly immediately before the test at a separate workspace with a dedicated pipette set and filter tips. The 96-well PCR plate containing the RT-LAMP mix was covered with an Society for Biomolecular Screening (SBS) plate lid. To avoid mix-ups during sample addition through well-by-well pipetting, the RNA or swab specimens were first collected into a 96-well seed plate. The RNA was then added to the plate with the LAMP reagents at a dedicated workspace with a manual 96-channel pipettor (Liquidator 20 μl, Mettler Toledo) using filter tips. The RT-LAMP and the RNA seed plate were instantly sealed with an optically clear adhesive seal (GK480-OS, Kisker Biotech) and an adhesive aluminum foil seal (SL-AM0550, Steinbrenner Laborsysteme, Germany), respectively. If the product of an RT-LAMP reaction had to be analyzed by gel electrophoresis, the plate was opened with extreme caution at a separated post-LAMP workspace and loaded onto an agarose gel with a dedicated pipette.\n\nRT-LAMP assay\nAssays were assembled in total reaction volumes of either 12.5 μl (for LAMP assays using isolated RNA) or 20 μl (for swab–to–RT-LAMP assays). Master mixes were prepared at room temperature for each reaction immediately before use with either 6.25 or 10 μl, respectively, of the WarmStart Colorimetric RT-LAMP 2X Master Mix (M1800, New England Biolabs) and 1.25 or 2 μl, respectively, of the 10× primer mix, filled up to 11.5 or 19 μl with nuclease-free water (AM9937, Ambion). Values given are for one reaction: For a 96-well plate, 100 times larger volumes were used, and the LAMP mix was distributed to the wells of a 96-well plate (4ti-0960/C, Brooks Life Sciences or 0030128672, Eppendorf) before pipetting 1 μl of sample into each well of the plate; for details, see previous paragraph. Plates were prepared immediately before use to limit exposure of the LAMP reagents to atmospheric CO2 (to prevent acidification of the reaction) and kept on an ice-cold metal block. Plates were sealed using a transparent adhesive foil (GK480-OS, Kisker Biotech), and the reactions were incubated in a PCR cycler at 65°C for 15 to 60 min with the lid heated to 75°C. To perform measurements at the indicated time points, the reactions were taken out of the PCR cycler and placed into an ice cold metal block for 30 s. This intensifies the color before the measurement. Photographs were taken with cell phone cameras or the scanner function of an office copying machine.\n\nQuantification of the RT-LAMP reaction\nAbsorbance measurements were performed with a Spark Cyto or Infinite M200 (Tecan) at 434 and 560 nm with 25 flashes. These two peaks from phenol red are strongly changing during the acidification of the reaction (434 nm absorbance is increased, 560 nm absorbance is decreased). To obtain a good readout of the color change, absorbance at 560 nm was substracted from the one at 434 nm. This difference was denoted ΔOD.\n\nSwab–to–RT-LAMP assay\nFor direct and hot swab–to–RT-LAMP assays, patient swab specimens were transferred first onto a 96-well seed plate. For the direct assay, we then transferred 1 μl of the specimen directly to 19 μl of LAMP mix per well in a ready-made 96-well PCR plate (0030128672, Eppendorf). The plate was sealed using a transparent adhesive foil (GK480-OS, Kisker Biotech) and kept on an ice-cold metal block. For the hot assay, we sealed the seed plate with a pierceable lid (4ti-0566/96, Brooks Life Sciences) and heated it in a PCR cycler for 5 min at 95°C (with the lid heated to 105°C). The seed plate was cooled down to 4°C on an ice-cold metal block. Afterward, 1 μl of the heat-treated patient specimens was quickly added to a second ready-made plate with 19 μl of LAMP mix per well. This plate was also sealed with transparent adhesive foil (GK480-OS, Kisker Biotech). Both plates were then incubated at 65°C for the LAMP reaction to proceed. For both swab–to–RT-LAMP assays, the PCR plates were briefly spun down and then incubated in a PCR cycler at 65°C for 10 to 60 min (with the lid heated to 75°C). To perform measurements at the indicated time points, the reactions were taken out of the PCR cycler and placed into an ice-cold metal block for 30 s.\n\nLAMP-sequencing method\nSequencing libraries for detecting viral sequences in RT-LAMP products were prepared by a modified Anchor-Seq protocol (37, 40) using Tn5 transposase tagmentation instead of sonication for genomic DNA fragmentation (17). The relevant primers are summarized in table S4.\nIn detail, transposon adapters containing well-defining barcodes and unique molecular identifiers (UMIs) were annealed by mixing 25 μM oligos (P5-UMI-xi5001…5096-ME.fw, Tn5hY-Rd2-Wat-SC3) in 5 μM tris-HCl (pH 8), incubating at 99°C for 5 min, and slowly cooling down to 20°C within 15 min in a thermocycler. Transposons were assembled by mixing Tn5(E54K, L372P) transposase (100 ng/μl) [purified according to (41)] with 1.25 μM annealed adapters in 50 mM Tris-HCl (pH 7.5) and incubating the reaction for 1 hour at 23°C. Tagmentation was carried out by mixing 1.2 μl of the RT-LAMP product (~200 ng DNA) with 1.5 μl of loaded transposase in freshly prepared tagmentation buffer [10 mM [tris(hydroxymethyl)methylamino]propanesulfonic acid) (TAPS)] (pH 8.5), 5 mM MgCl2, and 10% (v/v) dimethylformamide] using a Liquidator 96 Manual Pipetting System (Mettler Toledo). The reactions were incubated at 55°C for 10 min. Reactions were stopped by adding SDS to a final concentration of 0.033%. Tagmented DNA of each plate was pooled and size-selected using a two-step AMPureXP bead (Beckman Coulter) purification to target for fragments between 300 and 600 bp. First, 50 μl of pooled reaction was mixed with 50 μl of water and bound to 55 μl of beads to remove large fragments. To further remove small fragments, the supernatant of this reaction was added to 25 μl of fresh beads and further purified using two washes with 80% ethanol before the samples were finally eluted in 10 μl of 5 mM tris-HCl (pH 8). One PCR per plate with 1 μl of the eluate and RT-LAMP–specific and Tn5-adapter–specific primers (P7nxt-GeneN-A-LBrc and P7-xi7001..7016, P5.fw) was performed using NEBNext Q5 HotStart polymerase (New England Biolabs) with two cycles at 62°C for annealing and 90 s elongation, followed by two cycles at 65°C for annealing and 90 s elongation, and 13 cycles at 72°C annealing and 90 s elongation. All PCR reactions were combined and 19% of this pool was size-selected for 400 to 550 bp using a 2% agarose/tris-acetate-EDTA gel and column purification (Macherey-Nagel). The final sequencing library was quantified by qPCR (New England Biolabs) and sequenced with a paired-end sequencing run on a NextSeq 550 machine (Illumina) with 20% phiX spike-in and 136 cycles for the first read, 11 cycles to read the 11-nt-long plate index (i7) and 20 cycles to read the 11-nt-long well index (i5) and the 9-nt-long UMI.\nFor trimming of the reads (i.e., removal of P7 Illumina adapter sequences), cutadapt (version 2.8) (42) was used. For validation of the origin of the sequence of the LAMP product (fig. S4A), 107 reads were randomly selected and used for the analysis. Reads were mapped to the SARS-CoV-2 reference genome (NC_045512.2) (43), using bwa-mem with default settings (version 0.7.17-r1188) (44). Virus genome coverage was determined with the samtools depth command (version 1.10) (45). Using bwa-mem, 80.6% of reads could be mapped to the virus genome (fig. S4, B and C). To analyze the remaining sequences, a k-mer analysis using a custom script was performed. Using 9-mers, this matched 93.5% of the nonmapped reads with a maximal Levenshtein distance of two to one of the LAMP primers or their reverse complement sequences (fig. S4D). This is explained by the fact that LAMP products can consist of complex sequence rearrangements.\nFor classification of samples by LAMP-sequencing, reads were assigned to wells and counted using custom scripts. A read was considered as a match to SARS-CoV-2 N gene if at least one of three short sequences (~13 nt, marked orange in fig. S4A) not covered by RT-LAMP primers was found in the read, otherwise it was counted as unmatched. Sequencing reads were grouped by UMI and by position of the matched sequence with the aim of removing PCR duplicates. A sample was considered if more than 200 total UMIs were observed and called positive if more than 10,000 virus-matching UMIs were observed.\nThere is a very wide gap in the number of virus-matching reads between positive and negative samples (fig. S5A): The count is either below 7000 UMIs or above 45,000 UMIs. This is why we placed the decision threshold for scoring a sample as LAMP-sequencing positive within this gap. The fact that also RT-qPCR–negative samples give rise to some UMI counts containing viral sequences is explained by template switching of unattached adapters that remain in the reaction after tagmentation, but no cause for concern due to the wide gap between negative and positive samples.\nFor a few samples, we saw so few reads (less than 200 UMIs) that we suspected that the multiplexing had failed and excluded them from the results. As most of these were in the same row of the same plate, we analyzed these samples after LAMP-sequencing by gel electrophoresis (fig. S5B) to check for DNA content after RT-LAMP. We found that the gel results agree with the RT-LAMP outcome, indicating that the failure likely was caused later, probably during multiplexing.\n\nStatistical analysis\nExcept where otherwise noted, all data were analyzed with R (46) using the tidyverse (47) and ggplot2 (48) system or with GraphPad Prism. Sensitivity and specificity values were obtained from count tables as follows: Specificity of the RT-LAMP assay was calculated as the fraction of RT-qPCR–negative samples that were also negative in the RT-LAMP assay. Sensitivity for a given CT interval was calculated as the fraction of all samples with an RT-qPCR CT value in that interval that was positive in the RT-LAMP assay. In both cases, 95% confidence intervals were calculated by interpreting the fractions of counts as binomial rates and then using Wilson’s method for binomial confidence intervals as implemented in the R package binom (49). The R code used to perform analyses and produce figures can be found on GitHub, together with all data tables: 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