{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2023,1,29]],"date-time":"2023-01-29T05:22:38Z","timestamp":1674969758888},"reference-count":39,"publisher":"Oxford University Press (OUP)","issue":"19","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Motivation: Pyrosequencing technology provides an important new approach to more extensively characterize diverse sequence populations and detect low frequency variants. However, the promise of this technology has been difficult to realize, as careful correction of sequencing errors is crucial to distinguish rare variants (\u223c1%) in an infected host with high sensitivity and specificity.<\/jats:p>\n               <jats:p>Results: We developed a new approach, referred to as Indel and Carryforward Correction (ICC), to cluster sequences without substitutions and locally correct only indel and carryforward sequencing errors within clusters to ensure that no rare variants are lost. ICC performs sequence clustering in the order of (i) homopolymer indel patterns only, (ii) indel patterns only and (iii) carryforward errors only, without the requirement of a distance cutoff value. Overall, ICC removed 93\u201395% of sequencing errors found in control datasets. On pyrosequencing data from a PCR fragment derived from 15 HIV-1 plasmid clones mixed at various frequencies as low as 0.1%, ICC achieved the highest sensitivity and similar specificity compared with other commonly used error correction and variant calling algorithms.<\/jats:p>\n               <jats:p>Availability and implementation: Source code is freely available for download at http:\/\/indra.mullins.microbiol.washington.edu\/ICC. It is implemented in Perl and supported on Linux, Mac OS X and MS Windows.<\/jats:p>\n               <jats:p>Contact: \u00a0jmullins@uw.edu<\/jats:p>\n               <jats:p>Supplementary information: \u00a0Supplementary data are available at Bioinformatics online.<\/jats:p>","DOI":"10.1093\/bioinformatics\/btt434","type":"journal-article","created":{"date-parts":[[2013,7,31]],"date-time":"2013-07-31T00:34:28Z","timestamp":1375230868000},"page":"2402-2409","source":"Crossref","is-referenced-by-count":14,"title":["Indel and Carryforward Correction (ICC): a new analysis approach for processing 454 pyrosequencing data"],"prefix":"10.1093","volume":"29","author":[{"given":"Wenjie","family":"Deng","sequence":"first","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Brandon S.","family":"Maust","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Dylan H.","family":"Westfall","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Lennie","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Hong","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Brendan B.","family":"Larsen","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Shyamala","family":"Iyer","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"Yi","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]},{"given":"James I.","family":"Mullins","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington School of Medicine, Seattle, WA 98195, USA"}]}],"member":"286","published-online":{"date-parts":[[2013,7,29]]},"reference":[{"key":"2023012810462811400_btt434-B1","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool J","volume":"215","author":"Altschul","year":"1990","journal-title":"Mol. Biol."},{"key":"2023012810462811400_btt434-B2","doi-asserted-by":"crossref","first-page":"e1001022","DOI":"10.1371\/journal.pcbi.1001022","article-title":"The evolutionary analysis of emerging low frequency HIV-1 CXCR4 using variants through time\u2014an ultra-deep approach","volume":"6","author":"Archer","year":"2010","journal-title":"PLoS Comput. Biol."},{"key":"2023012810462811400_btt434-B3","doi-asserted-by":"crossref","first-page":"8247","DOI":"10.1128\/JVI.00897-09","article-title":"Ultradeep pyrosequencing detects complex patterns of CD8+ T-lymphocyte escape in simian immunodeficiency virus-infected macaques","volume":"83","author":"Bimber","year":"2009","journal-title":"J. Virol."},{"key":"2023012810462811400_btt434-B4","doi-asserted-by":"crossref","first-page":"12087","DOI":"10.1128\/JVI.01378-10","article-title":"Whole-genome characterization of human and simian immunodeficiency virus intrahost diversity by ultradeep pyrosequencing","volume":"84","author":"Bimber","year":"2010","journal-title":"J. Virol."},{"key":"2023012810462811400_btt434-B5","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1038\/nmeth.1990","article-title":"Fast, accurate error-correction of amplicon pyrosequences using Acacia","volume":"9","author":"Bragg","year":"2012","journal-title":"Nat. Methods"},{"key":"2023012810462811400_btt434-B6","doi-asserted-by":"crossref","first-page":"13088","DOI":"10.1128\/JVI.05650-11","article-title":"Pyrosequencing reveals restricted patterns of CD8+ T cell escape-associated compensatory mutations in simian immunodeficiency virus","volume":"85","author":"Burwitz","year":"2011","journal-title":"J. Virol."},{"key":"2023012810462811400_btt434-B7","doi-asserted-by":"crossref","first-page":"e1000074","DOI":"10.1371\/journal.pcbi.1000074","article-title":"Viral population estimation using pyrosequencing","volume":"4","author":"Eriksson","year":"2008","journal-title":"PLoS Comput. Biol."},{"key":"2023012810462811400_btt434-B8","doi-asserted-by":"crossref","first-page":"e12303","DOI":"10.1371\/journal.pone.0012303","article-title":"Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing","volume":"5","author":"Fischer","year":"2010","journal-title":"PLoS One"},{"key":"2023012810462811400_btt434-B9","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1186\/1471-2164-12-245","article-title":"Accuracy and quality assessment of 454 GS-FLX Titanium pyrosequencing","volume":"12","author":"Gilles","year":"2011","journal-title":"BMC genomics"},{"key":"2023012810462811400_btt434-B10","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511574931","volume-title":"Algorithms on Strings, Trees, and Sequences: Computer Science and Computational Biology","author":"Gusfield","year":"1997"},{"key":"2023012810462811400_btt434-B11","doi-asserted-by":"crossref","first-page":"e11345","DOI":"10.1371\/journal.pone.0011345","article-title":"Dynamics of HIV-1 quasispecies during antiviral treatment dissected using ultra-deep pyrosequencing","volume":"5","author":"Hedskog","year":"2010","journal-title":"PLoS One"},{"key":"2023012810462811400_btt434-B12","doi-asserted-by":"crossref","first-page":"e1002529","DOI":"10.1371\/journal.ppat.1002529","article-title":"Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection","volume":"8","author":"Henn","year":"2012","journal-title":"PLoS Pathog"},{"key":"2023012810462811400_btt434-B13","doi-asserted-by":"crossref","first-page":"7523","DOI":"10.1128\/JVI.02697-10","article-title":"Demographic processes affect HIV-1 evolution in primary infection before the onset of selective processes","volume":"85","author":"Herbeck","year":"2011","journal-title":"J. Virol."},{"key":"2023012810462811400_btt434-B14","doi-asserted-by":"crossref","first-page":"R143","DOI":"10.1186\/gb-2007-8-7-r143","article-title":"Accuracy and quality of massively parallel DNA pyrosequencing","volume":"8","author":"Huse","year":"2007","journal-title":"Genome Biol."},{"key":"2023012810462811400_btt434-B15","doi-asserted-by":"crossref","first-page":"1889","DOI":"10.1111\/j.1462-2920.2010.02193.x","article-title":"Ironing out the wrinkles in the rare biosphere through improved OTU clustering","volume":"12","author":"Huse","year":"2010","journal-title":"Environ. Microbiol."},{"key":"2023012810462811400_btt434-B16","doi-asserted-by":"crossref","first-page":"5802","DOI":"10.1128\/JVI.00117-10","article-title":"Mathematical modeling of ultradeep sequencing data reveals that acute CD8+ T-lymphocyte responses exert strong selective pressure in simian immunodeficiency virus-infected macaques but still fail to clear founder epitope sequences","volume":"84","author":"Love","year":"2010","journal-title":"J. Virol."},{"key":"2023012810462811400_btt434-B17","doi-asserted-by":"crossref","first-page":"e1002417","DOI":"10.1371\/journal.pcbi.1002417","article-title":"Highly sensitive and specific detection of rare variants in mixed viral populations from massively parallel sequence data","volume":"8","author":"Macalalad","year":"2012","journal-title":"PLoS Comput. Biol."},{"key":"2023012810462811400_btt434-B18","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1038\/nature03959","article-title":"Genome sequencing in microfabricated high-density picolitre reactors","volume":"437","author":"Margulies","year":"2005","journal-title":"Nature"},{"key":"2023012810462811400_btt434-B20","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/0022-2836(70)90057-4","article-title":"A general method applicable to the search for similarities in the amino acid sequence of two proteins","volume":"48","author":"Needleman","year":"1970","journal-title":"J. Mol. Biol."},{"key":"2023012810462811400_btt434-B21","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1128\/JVI.05511-11","article-title":"Conditional CD8+ T cell escape during acute simian immunodeficiency virus infection","volume":"86","author":"O'Connor","year":"2012","journal-title":"J. Virol."},{"key":"2023012810462811400_btt434-B22","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1093\/molbev\/msp289","article-title":"Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of HIV-1","volume":"27","author":"Poon","year":"2010","journal-title":"Mol. Biol. Evol."},{"key":"2023012810462811400_btt434-B23","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1093\/bioinformatics\/btr627","article-title":"QuRe: software for viral quasispecies reconstruction from next-generation sequencing data","volume":"28","author":"Prosperi","year":"2012","journal-title":"Bioinformatics"},{"key":"2023012810462811400_btt434-B24","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1038\/nmeth.1361","article-title":"Accurate determination of microbial diversity from 454 pyrosequencing data","volume":"6","author":"Quince","year":"2009","journal-title":"Nat. Methods"},{"key":"2023012810462811400_btt434-B25","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/1471-2105-12-38","article-title":"Removing noise from pyrosequenced amplicons","volume":"12","author":"Quince","year":"2011","journal-title":"BMC Bioinformatics"},{"key":"2023012810462811400_btt434-B26","doi-asserted-by":"crossref","first-page":"e57615","DOI":"10.1371\/journal.pone.0057615","article-title":"PyroClean: denoising pyrosequences from protein-coding amplicons for the recovery of interspecific and intraspecific genetic variation","volume":"8","author":"Ramirez-Gonzalez","year":"2013","journal-title":"PLoS One"},{"key":"2023012810462811400_btt434-B27","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1038\/nmeth0910-668b","article-title":"Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions","volume":"7","author":"Reeder","year":"2010","journal-title":"Nat. Methods"},{"key":"2023012810462811400_btt434-B28","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1089\/aid.1997.13.737","article-title":"Quantitation of target molecules from polymerase chain reaction-based limiting dilution assays","volume":"13","author":"Rodrigo","year":"1997","journal-title":"AIDS Res. Hum. Retroviruses"},{"key":"2023012810462811400_btt434-B29","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.jviromet.2006.04.009","article-title":"Large-scale amplification, cloning and sequencing of near full-length HIV-1 subtype C genomes","volume":"136","author":"Rousseau","year":"2006","journal-title":"J. Virol. Methods"},{"key":"2023012810462811400_btt434-B30","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1093\/bioinformatics\/btr170","article-title":"Correcting errors in short reads by multiple alignments","volume":"27","author":"Salmela","year":"2011","journal-title":"Bioinformatics"},{"key":"2023012810462811400_btt434-B31","doi-asserted-by":"crossref","first-page":"257","DOI":"10.7326\/0003-4819-125-4-199608150-00001","article-title":"Clinical and epidemiologic features of primary HIV infection","volume":"125","author":"Schacker","year":"1996","journal-title":"Ann. Intern. Med."},{"key":"2023012810462811400_btt434-B32","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/1742-4690-10-18","article-title":"Analysis of 454 sequencing error rate, error sources, and artifact recombination for detection of Low-frequency drug resistance mutations in HIV-1 DNA","volume":"10","author":"Shao","year":"2013","journal-title":"Retrovirology"},{"key":"2023012810462811400_btt434-B33","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1086\/596736","article-title":"Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes","volume":"199","author":"Simen","year":"2009","journal-title":"J. Infect. Dis."},{"key":"2023012810462811400_btt434-B34","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1258\/ijsa.2011.011178","article-title":"Are there benefits to starting antiretroviral therapy during primary HIV infection? Conclusions from the Seattle Primary Infection Cohort vary by control group","volume":"23","author":"Stekler","year":"2012","journal-title":"Int. J. STD AIDS"},{"key":"2023012810462811400_btt434-B35","doi-asserted-by":"crossref","first-page":"e5683","DOI":"10.1371\/journal.pone.0005683","article-title":"Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo","volume":"4","author":"Tsibris","year":"2009","journal-title":"PLoS One"},{"key":"2023012810462811400_btt434-B36","doi-asserted-by":"crossref","first-page":"167","DOI":"10.2144\/000113733","article-title":"Minor variant detection in amplicons using 454 massive parallel pyrosequencing: experiences and considerations for successful applications","volume":"51","author":"Vandenbroucke","year":"2011","journal-title":"Biotechniques"},{"key":"2023012810462811400_btt434-B37","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1101\/gr.6468307","article-title":"Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance","volume":"17","author":"Wang","year":"2007","journal-title":"Genome Res."},{"key":"2023012810462811400_btt434-B38","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1186\/1471-2105-12-119","article-title":"ShoRAH: estimating the genetic diversity of a mixed sample from next-generation sequencing data","volume":"12","author":"Zagordi","year":"2011","journal-title":"BMC Bioinformatics"},{"key":"2023012810462811400_btt434-B39","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1089\/cmb.2009.0164","article-title":"Deep sequencing of a genetically heterogeneous sample: local haplotype reconstruction and read error correction","volume":"17","author":"Zagordi","year":"2010","journal-title":"J. Comput. Biol."},{"key":"2023012810462811400_btt434-B40","doi-asserted-by":"crossref","first-page":"7400","DOI":"10.1093\/nar\/gkq655","article-title":"Error correction of next-generation sequencing data and reliable estimation of HIV quasispecies","volume":"38","author":"Zagordi","year":"2010","journal-title":"Nucleic Acids Res."}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/29\/19\/2402\/48890726\/bioinformatics_29_19_2402.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/29\/19\/2402\/48890726\/bioinformatics_29_19_2402.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,28]],"date-time":"2023-01-28T12:34:02Z","timestamp":1674909242000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/29\/19\/2402\/191707"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,7,29]]},"references-count":39,"journal-issue":{"issue":"19","published-print":{"date-parts":[[2013,10,1]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btt434","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2013,10,1]]},"published":{"date-parts":[[2013,7,29]]}}}